ANIMAL BEHAVIOUR, 2008, 75, 921e927

doi:10.1016/j.anbehav.2007.07.023

Available online at www.sciencedirect.com

Imprinted species recognition lasts for life in free-living

great tits and blue tits
BO TERNING H ANSEN, LAR S ERIK JOHA NNESS EN & T ORE SLA GS VOLD

Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo
(Received 16 March 2007; initial acceptance 17 June 2007;
nal acceptance 16 July 2007; published online 29 October 2007; MS. number: 9314)

Species recognition may be learned through imprinting early in life. Imprinting has normally been studied
under highly unnatural conditions in the laboratory. We tested whether species recognition mediated
through imprinting is individually modiable in a eld setting where great tits, Parus major, have been
articially cross-fostered to blue tits, Cyanistes caeruleus, and vice versa. We have shown previously that
cross-fostered birds have deviant species recognition, in terms of both mate choice and aggressive responses towards rivals. Natural interactions among conspecics and heterospecics are common in these
populations, potentially giving cross-fostered birds scope for relearning their species identity. We tested
whether species recognition may change with experience during adulthood by comparing the aggressive
response of cross-fostered birds and controls of different ages towards caged intruders. When breeding,
cross-fostered birds responded aggressively towards same-sex individuals of their heterospecic foster species, while unmanipulated controls responded mainly towards conspecics. We found that the aggressive
response decreased with age at similar rates in both treatments and in both species. Moreover, there was no
effect of age on the relative response towards conspecics and heterospecics in either treatment. Hence,
we found no evidence that the species recognition behaviour towards same-sex individuals is shifted towards conspecics with age in interspecically cross-fostered birds. We conclude that species recognition
is irreversible once it has been established in free-living great tits and blue tits. This is the rst study to
investigate the stability of species recognition in the eld.
2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: aggression; blue tit; Cyanistes caeruleus; early learning; great tit; imprinting; Parus major; rival imprinting;
species recognition; territoriality

Many animals learn to recognize their own species

through imprinting. Imprinting is a learning process
characterized by a relatively short sensitive phase occurring early in development, and its effects are long lasting
(Lorenz 1937; Hess 1973). In species with parental care the
process seems to be widespread; it has been well documented in birds (reviewed in ten Cate & Vos 1999) and
has been shown also in mammals (Kendrick et al. 1998;
Penn & Potts 1998) and sh (Verzijden & ten Cate 2007).
Imprinting has been studied mainly in terms of the
following-response of precocial birds (lial imprinting,
e.g. Gottlieb 1971) and the development of sexual preferences (sexual imprinting, e.g. ten Cate et al. 2006). The

Correspondence: B. T. Hansen, Department of Biology, Centre for

Ecological and Evolutionary Synthesis, University of Oslo, P.O. Box
1066 Blindern, NO-0316 Oslo, Norway (email: b.t.hansen@bio.uio.no).
0003e 3472/08/$32.00/0

process is also applicable to the recognition of same-sex

individuals (rival imprinting, Hansen & Slagsvold 2003).
Learning by imprinting was originally thought to be
irreversible (Lorenz 1937). Early reports on the stability of
species preferences over time were anecdotal (reviewed in
Bateson 1966; Immelmann 1972a). In the rst known
study to investigate experimentally the stability of mate
preferences over several years, captive male zebra nches,
Taeniopygia guttata, raised by Bengalese nch, Lonchura
striata, parents in the laboratory preferred to mate with
Bengalese nch females over several breeding attempts,
even after extensive experience with conspecics (Immelmann 1972b).
More recent laboratory experiments on the zebra nch,
however, have shown that mate preferences may be
malleable until the experience of rst courtship. Birds
raised by heterospecic foster parents develop a preference
for individuals of their foster species if they also

921
2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

922

ANIMAL BEHAVIOUR, 75, 3

experience their rst courtship with individuals of that

foster species, but if such cross-fostered birds are exposed
to conspecics during rst courtship or breeding, they
may shift their initial preference towards conspecics
(Bischof & Clayton 1991; Immelmann et al. 1991; Kruijt
& Meeuwissen 1991; see also Kruijt & Meeuwissen 1993;
Oetting et al. 1995; Oetting & Bischof 1996). These ndings have been corroborated by studies of the zebra nch
forebrain, where physical changes accompany the early
experiences as well as the experiences during rst courtship (reviewed in Bischof 2003). Thus sexual imprinting
appears to be accomplished in two stages.
We have interspecically cross-fostered wild great tits,
Parus major, and blue tits, Cyanistes caeruleus, over several
years and established that their species recognition is
inuenced by cross-fostering in terms of both mate preferences (Slagsvold et al. 2002) and recognition of same-sex
rivals (Hansen & Slagsvold 2003) in the eld. In the present study we aimed to investigate the stability of this acquired species identity by comparing how the aggressive
behaviour of cross-fostered and control tits may change
with age. To our knowledge, the stability of imprinting
has never before been experimentally investigated in the
wild. Great tits and blue tits differ in appearance and behaviour, but have similar feeding and habitat preferences
and form mixed-species ocks outside the breeding season
(e.g. Hinde 1952). Interspecic and intraspecic interactions are hence very common among these social tits.
Interspecically cross-fostered birds may shift their preference towards conspecics if they possess some inherent
own-species bias (Immelmann 1972a; Sonnemann &
lander 1977; Immelmann & Suomi 1981; Bischof &
Sjo
Clayton 1991). Also, cross-fostered birds might have
learned from interacting with conspecics and heterospecics and may consequently have changed their behaviour
(Bossema & Kruijt 1982; Kruijt et al. 1982; ten Cate 1984;
ten Cate & Mug 1984).

METHODS

General Field Procedures

We conducted the study in a 1.6-km2 plot containing
some 450 nestboxes at Dli, near Oslo, Norway. Great
tits and blue tits have been interspecically cross-fostered
here since 1995 (i.e. researchers have articially transferred eggs between nests of these two species). Crossfostered individuals thrive in the nests of their hosts, but
their adult behaviour differs from that of controls of their
own species (Slagsvold et al. 2002; Hansen & Slagsvold
2003). We keep track of the local great tit and blue tit populations through individual colour banding of recruits.
Nearly all great tits and blue tits breeding in the study
area use the provided nestboxes.
We assigned birds to two treatment groups. (1) Control
birds were unmanipulated and were raised by unmanipulated parents. (2) Cross-fostered birds were raised by
unmanipulated heterospecic parents (great tit foster
parents for blue tit chicks and vice versa). For a more

detailed account of the general eld procedures, see Slagsvold et al. (2002).

Cage Experiment
To determine aggressive responses, we exposed focal
birds to simulated territorial intrusions during the breeding season in 1999e2006. We sequentially presented focal
birds with a live, caged great tit or blue tit near their
nestbox between the onset of nest building and the start
of incubation (1.1  4.8, mean  SD, days after laying of
the rst egg). Focal and stimulus birds were always of
the same sex. We allowed at least 1 h between the two trials, and we randomized the order of presentation. We
recorded the response of the focal bird as the time spent
within 2 m of the cage during a 5-min trial. Close proximity to the simulated intruder is most often accompanied
by clearly aggressive behaviour in terms of posture, chase
ights, etc. Thus, 64.5  36.9% of the time spent within
2 m of the cage was spent in physical contact with the
cage. We began trials immediately after the observer conrmed that the resident focal bird was aware of the caged
intruder, with the criteria that the focal bird had an unobstructed view to the stimulus bird and had its attention
directed towards the cage.
To ensure that stimulus birds (N 110) were unfamiliar
to focal birds, they were caught outside the nestbox plot.
While in captivity, we supplied them with meal worms
and water ad libitum. To balance the evils of keeping
a large number of birds captive and engaging in stimulus
pseudoreplication, we used most stimulus birds twice
within each treatment group (1.7  0.9). We held stimulus
birds captive for 3.3  2.9 days and released them at the
site of capture. During trials, stimulus birds apparently
avoided the response bird, at least when the latter perched
on the cage. Physical contact between the birds was hindered by the cage, as well as by the movements of the
stimulus bird. We have never observed a stimulus bird to
be injured as a consequence of the experimental trials.
None of the stimulus birds died in captivity. The reproduction of stimulus birds could be negatively affected because
most were territorial at capture. Potential effects include
delayed reproduction, displacement from their original
territory and disruption of pair bonds. Stimulus birds
were caught before the initiation of reproduction (while
roosting in empty nestboxes), during nest building or during the early stages of egg laying (in mist nets). In this part
of Norway, initiation of egg laying extends to the middle
of June for both species of tits, while the termination
date for our experiment was 19 May 6.6 days. Although
we did not have the capacity to monitor stimulus birds
after release, we subsequently observed several breeding.
For more details regarding the cage experiments and
ethical issues relating to the cross-fostering procedure,
see Hansen & Slagsvold (2003).

Statistics
The complete data set contained 312 individuals (85
control blue tits, 82 cross-fostered blue tits, 79 control

HANSEN ET AL.: STABILITY OF LEARNED SPECIES RECOGNITION

blue tits, controls and cross-fostered birds responded similarly, while great tit controls responded more strongly
than cross-fostered birds towards conspecic intruders
(Fig. 1). Furthermore, there was a signicant decrease in
aggressive response with increasing age (F1,78 13.08,
P 0.001). The effect of age tended to differ between
treatments (F1,78 2.66, P 0.11), and there tended to
be a species difference in the interaction between age
and treatment (F2,78 2.65, P 0.08). Interaction plots
(Fig. 1) suggest that in blue tits the reduced aggressive
response with age towards conspecics did not differ
between the treatments, while in great tits controls

100 (a)

80

60

40

Conspecific aggressive response (%)

great tits, 66 cross-fostered great tits), of which 254

individuals were trialled in one breeding season only,
and 58 individuals were trialled in at least two breeding
seasons (8 control blue tits, 22 cross-fostered blue tits, 13
control great tits, 15 cross-fostered great tits). In total there
were 394 observations per model on the complete data set
(Table 1).
We performed separate analyses for aggressive responses towards conspecics and heterospecics and
a ratio between the two types of stimuli. The response
ratio was calculated as [response towards conspecics/
(response towards conspecics response towards
heterospecics)]  100. A response ratio of 50% thus
means that the responses towards conspecics and heterospecics are equal, a higher ratio means that aggressive
responses are stronger towards conspecics than towards
heterospecics and a lower ratio means the opposite.
Birds that spent no time within 2 m of the cage in either
of the two trials were given a response ratio of 50%.
To avoid pseudoreplicating the response of the same
individuals trialled in several breeding seasons, we used
mixed models to analyse the potential change with age in
aggressive response towards conspecics and heterospecics (Pinheiro & Bates 2000). Initial models were tted
with xed effects for species, sex, treatment, age and the
interactions species:age, sex:age, treatment:age, treatment:species, treatment:species:age (entered in that order)
and with random effect for individual. Initial models were
reduced by backwards elimination. Models were tted
with both equal and unequal variances between factor
levels and with random effects for intercept only and for
intercept and slope. Alternative models were compared
in likelihood-ratio tests with maximum likelihood ts,
and the most parsimonious model was in each case selected. However, the interaction between treatment and
age was always retained in the model whether or not it
improved model t. Model parameters were estimated by
restricted maximum likelihood. Alternative hypotheses
were not directional, and the a level was 0.05. Statistical
modelling was performed with R 2.4.0 (R Development
Core Team 2006).

20

100 (b)

80

60

RESULTS
The aggressive response towards conspecic intruders was
stronger in blue tits than in great tits (F1,308 160.21,
P < 0.0001) and stronger in controls than in cross-fostered
birds (F1,308 7.35, P 0.007), but the treatment effect
differed between species (F1,308 24.98, P < 0.0001). In

40

20

Table 1. Number of observations by age, species and treatment

Age (years)

Great tit control

Great tit cross-fostered
Blue tit control
Blue tit cross-fostered

46
45
63
68

26
22
21
26

10
14
8
16

10
4
3
5

2
3
1
0

0
1
0
0

3
Age (years)

Figure 1. Change in mean  SE aggressive response with age towards conspecific intruders for cross-fostered (C, solid regression
line) and control (O, dashed regression line) (a) great tits and (b)
blue tits. Aggressive response is measured as the proportion of
5 min spent within 2 m of a caged conspecific intruder. Number of
observations is given in Table 1.

923

ANIMAL BEHAVIOUR, 75, 3

reduced their response with age to a greater extent than

did cross-fostered birds.
Blue tits responded more aggressively than great tits
towards
heterospecic
intruders
(F1,308 18.04,
P < 0.0001) and cross-fostered birds responded more aggressively than controls (F1,308 131.29, P < 0.0001), but
the effect of treatment was not equal in the two species
(F1,308 22.82, P < 0.0001). In both species, cross-fostered
birds responded more than controls, but the magnitude of
this difference was greater in blue tits than in great tits
(Fig. 2). The model of aggressive response towards

100 (a)

80

60

40
Heterospecific aggressive response (%)

924

20

0
1

100 (b)

80

heterospecics further showed a decrease in response

with increasing age (F1,80 15.64, P 0.0002; Fig. 2). Importantly, the effect of age was similar for controls and
cross-fostered birds (F1,80 0.98, P 0.33).
The response towards conspecics relative to that
towards heterospecics (i.e. the response ratio) differed
between the species (F1,309 26.65, P < 0.0001), with blue
tits responding more towards conspecics than heterospecics compared to great tits. Controls responded relatively
more towards conspecics than towards heterospecics in
comparison with cross-fostered birds (F1,309 206.11,
P < 0.0001). However, there was no effect of age on the response ratio (F1,80 0.47, P 0.50) because the rates of
decline in aggressive response with age were similar in
the responses towards both conspecics and heterospecics. Furthermore, there was no interaction between
treatment and age (F1,80 0.28, P 0.60); hence both
controls and cross-fostered birds showed a similar lack of
effect of age on the response towards conspecics relative
to the response towards heterospecics (Fig. 3).
Because the cross-fostered birds responses to heterospecics seem similar to the controls responses to conspecics, comparing the aggressive response towards
conspecics for controls and the aggressive response
towards heterospecics for cross-fostered birds is justied.
The model shows that blue tits responded more aggressively than great tits (F1,309 59.23, P < 0.0001) and that
controls responded somewhat more than cross-fostered
birds (F1,309 5.88, P 0.02). Again, aggression waned
with age (F1,79 25.75, P < 0.0001), and this happened
at a faster rate in great tits than in blue tits (F1,79 7.07,
P 0.01). Note, however, that there was no difference
between controls and cross-fostered birds in the rate of
declining aggressive response with age (F1,79 0.22,
P 0.64). Hence, cross-fostered birds did not respond
less towards heterospecics with increasing age than did
controls towards conspecics.
We also performed separate analyses on the 58 birds
trialled in several breeding seasons (Tables A1 and A2 in
the Appendix). These analyses conrmed our main
ndings.

60

DISCUSSION
40

20

0
1

3
Age (years)

Figure 2. Change in mean  SE aggressive response with age towards heterospecific intruders for cross-fostered (C, solid regression
line) and control (O, dashed regression line) (a) great tits and (b)
blue tits. Aggressive response is measured as the proportion of
5 min spent within 2 m of a caged heterospecific intruder. Number
of observations is given in Table 1.

Cross-fostered birds responded more to heterospecics

than did controls, and cross-fostered great tits responded
less towards conspecics than did controls, while both
cross-fostered and control blue tits responded highly
aggressively towards conspecics. These results conrm
those from a previous study with a smaller sample
(Hansen & Slagsvold 2003). We show that these differences between controls and cross-fostered birds are quite
robust with increasing age. The aggressive response decreases with age at a similar rate in both treatments and
in both species and in response towards conspecics as
well as heterospecics. Hence, although the absolute level
of aggression changes with age, differences between controls and cross-fostered birds persist. Consequently, the
response towards conspecics relative to that towards heterospecics appears unaffected by age for both treatments.

HANSEN ET AL.: STABILITY OF LEARNED SPECIES RECOGNITION

100 (a)

80

60

Aggressive response ratio (%)

40

20

0
1

100 (b)

80

60

40

20

0
1

3
Age (years)

Figure 3. Change in mean  SE aggressive response ratio with age

towards conspecific relative to heterospecific intruders for crossfostered (C, solid regression line) and control (O, dashed regression
line) (a) great tits and (b) blue tits. Aggressive response ratio is measured as the response to the heterospecific divided by the sum of the
responses to the heterospecific and conspecific intruders. Number of
observations is given in Table 1.

Hence, interspecically cross-fostered great tits and blue

tits become imprinted on their foster species, and this
learned species recognition is not shifted towards conspecics during adulthood. The original imprinting thus
seems to persist throughout life, even though the crossfostered birds have had unlimited opportunities to interact with both conspecics and heterospecics.
Blue tits are more responsive than great tits to the
presentation of caged intruders. One of the models also
indicates that the negative effect of age on aggression may

be stronger in great tits than in blue tits. Blue tits are

known for their ery temper (Colquhoun 1942), and our
general impression is that great tits are somewhat more
shy than blue tits. This may explain the observed species
differences in aggressive response. Another general nding is that the aggressive response declines with age. We
think that experienced birds improve in identifying real
threats and may respond less to a caged intruder presented
by a human. Furthermore, older birds may have higher
status and thus deem a ght unnecessary to defend their
interests, or they may simply have less ghting ability
than younger birds. It is also possible that shy birds live
longer and that we observe a population increase in shy
birds rather than an age-effect per se. The birds used in
several years represent a sample of relatively old birds.
Hence, if shyness is important, we expect no age-effect
and a low aggressive response as yearlings for these birds.
This is not the case, which indicates that we are in fact
observing an effect of age.
The aggressiveness of great tit controls towards conspecics decreases at a faster rate than is the case for crossfostered birds. We do not know what causes this
difference. However, control yearlings have a high response while cross-fostered yearlings have a low response
towards conspecics. Control great tits thus have a greater
scope for a decrease in aggressiveness with age than do
cross-fostered great tits.
Evidence from studies on captive birds indicates that
mate preferences may change with experience until the
event of rst courtship/mate choice (Bossema & Kruijt
1982; Kruijt et al. 1982; ten Cate et al. 1984; Bischof &
Clayton 1991; Immelmann et al. 1991; Kruijt & Meeuwissen 1991, 1993; Oetting et al. 1995; Oetting & Bischof
1996). The results on the potential effects of experience
beyond rst mate choice are somewhat less clear-cut.
Adult mate preferences of males remain stable
(Immelmann 1972a; Immelmann et al. 1991; Kruijt &
Meeuwissen 1991, 1993; Oetting & Bischof 1996), while
the preferences of cross-fostered females may shift towards
conspecics with increasing age (ten Cate & Mug 1984).
From these laboratory studies one can conclude that the
acquired preferences of zebra nches cross-fostered to
Bengalese nches are unstable until rst courtship, but remain quite stable thereafter, and that there might be some
scope for change even after rst courtship, given certain
experimental conditions.
Tits breeding in our study area encounter nonfamiliar
conspecics and heterospecics almost immediately after
edging, because the breeding populations are dense
(about one tit pair/ha) and most broods edge within
a week of each other. These tits are social throughout life
and form mixed-species ocks during late summer, autumn and winter (Perrins 1979). Aggressive interactions
over food, both intra- and interspecically, are common.
The larger great tits are dominant over blue tits, and males
are dominant over females (Hansen & Slagsvold 2004). In
such a system species recognition is not likely to be consolidated during rst courtship, because edglings are
not likely to experience courtship until the following
breeding season, and they must be able to distinguish between species as well as sexes in the many interactions

925

926

ANIMAL BEHAVIOUR, 75, 3

they are bound to experience during their rst summer,

autumn and winter. Repeated errors in this respect will
probably be costly. Hence, stable species recognition based
on the initial imprinting on parental characteristics
should be established early in the life of these tits. We suggest that if courtship behaviour inuences mate recognition under natural circumstances in social species such
as tits, the formation of the species recognition that is
functional during the nonbreeding season must be separate from the species recognition conrmed through
mate choice (see also Bischof 2003).
Interestingly, the outcome of the misdirected aggression
does not seem to inuence species recognition. In winter,
cross-fostered great tits generally win aggressive interactions over food against blue tits, while cross-fostered blue
tits lose against great tits (Hansen & Slagsvold 2004). Nevertheless, this study shows that cross-fostered birds of
both species retain the mistaken species recognition;
hence blue tits do not become any wiser from losing
than great tits become from winning.
Several authors have observed that interspecically
cross-fostered individuals prefer conspecics and have
interpreted this phenomenon as an own-species bias (e.g.
Klint 1975). However, an alternative explanation for some
of these ndings is that the cross-fostered individuals may
not have been able to choose freely, but instead have responded to the individuals courting them most intensely,
which in most cases will be conspecics (e.g. Bossema &
Kruijt 1982). This is likely to apply to the tits in the present
study as well. Sometimes a cross-fostered great tit and
a cross-fostered blue tit of opposite sex meet and form a heterospecic pair (Slagsvold et al. 2002). However, most birds,
irrespective of treatment, are more likely to be courted by
conspecics because unmanipulated birds outnumber
cross-fostered birds. Judging from the aggressive response
towards intruders of both species, courtship experiences
with conspecics have not corrected the species recognition of cross-fostered birds, because even those breeding
with conspecics show the same pattern of aggressive response as other cross-fostered birds (Hansen et al. 2007).
In conclusion, acquired species recognition of wild great
tits and blue tits seems to be irreversible once it has been
established. Extensive experience from natural interactions with conspecics and heterospecics throughout life
does not seem to affect species recognition. The vast
majority of studies on imprinting have been performed
in the laboratory under extremely unnatural conditions.
This eld study enhances understanding of the natural
function of this learning process. This is also the rst time
that the stability of imprinted species recognition has
been investigated in terms of same-sex species recognition. Surprisingly, the development of rival recognition
has been almost completely overlooked in previous
studies on imprinting.

Acknowledgments
We thank everyone who helped us in the eld, the
Vestgard family for permission to work on their premises,
Leif C. Stige for statistical advice and two anonymous

referees for comments on a previous version of the

manuscript. The Research Council of Norway funded
grants for L.E.J. and B.T.H. The study complied with
Norwegian law and was conducted under licences from
the Directorate for Nature Management and the National
Animal Research Authority in Norway.

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Appendix
Table A1. ANCOVA results for fixed model terms from a mixed model
with individual as random effect and aggressive response of great tits
and blue tits towards conspecific intruders as dependent variable

Intercept
Species
Treatment
Age
Treatment*age
Treatment*species

df

1,79
1,54
1,54
1,79
1,79
1,54

380.39
71.89
3.34
15.28
1.19
5.35

<0.0001
<0.0001
0.07
0.0002
0.28
0.02

The sample is restricted to birds used in at least two breeding

seasons.
Table A2. ANCOVA results for fixed model terms from a mixed
model with individual as random effect and aggressive response of
great tits and blue tits towards heterospecific intruders as dependent
variable

Intercept
Species
Treatment
Age
Treatment*age
Treatment*species

df

1,79
1,54
1,54
1,79
1,79
1,54

159.68
15.32
32.21
14.38
0.06
12.36

<0.0001
0.0003
<0.0001
0.0003
0.81
0.0009

The sample is restricted to birds used in at least two breeding

seasons.

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