Available online at ww

w.sciencedirect.com

ANIMAL BEHAVIOUR, 2008, 75, 921e927doi:10.1016/j.anbehav.2007.07.023

Imprinted species recognition lasts for life in free-living

great tits and blue tits

BO TERNING HANSEN, LARS ERIK JOHANNESSEN & TORE SLAGSVOLD

Department of Biology, Centre for Ecological and Evolutionary Synthesis, University of Oslo

(Received 16 March 2007; initial acceptance 17 June 2007;

final 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 studiedunder highly unnatural conditions in the laboratory. We tested whether species recognition mediatedthrough imprinting is individually modifiable in a field setting where great tits, Parus major, have beenartificially cross-fostered to blue tits, Cyanistes caeruleus, and vice versa. We have shown previously thatcross-fostered birds have deviant species recognition, in terms of both mate choice and aggressive re-sponses towards rivals. Natural interactions among conspecifics and heterospecifics are common in thesepopulations, potentially giving cross-fostered birds scope for relearning their species identity. We testedwhether species recognition may change with experience during adulthood by comparing the aggressiveresponse 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 heterospecific foster spe-cies, while unmanipulated controls responded mainly towards conspecifics. We found that the aggressiveresponse decreased with age at similar rates in both treatments and in both species. Moreover, there was noeffect of age on the relative response towards conspecifics and heterospecifics in either treatment. Hence,we found no evidence that the species recognition behaviour towards same-sex individuals is shifted to-wards conspecifics with age in interspecifically cross-fostered birds. We conclude that species recognitionis irreversible once it has been established in free-living great tits and blue tits. This is the first study toinvestigate the stability of species recognition in the field.

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

Keywords: aggression; blue tit; Cyanistes caeruleus; early l

CorrespEcologic1066 Bli

0003e3

earning; great tit; imprinting; Parus major; rival imprinting;species recognition; territoriality

Many animals learn to recognize their own species process is also applicable to the recognition of same-sex

through imprinting. Imprinting is a learning processcharacterized by a relatively short sensitive phase occur-ring early in development, and its effects are long lasting(Lorenz 1937; Hess 1973). In species with parental care theprocess seems to be widespread; it has been well docu-mented in birds (reviewed in ten Cate & Vos 1999) andhas been shown also in mammals (Kendrick et al. 1998;Penn & Potts 1998) and fish (Verzijden & ten Cate 2007).

Imprinting has been studied mainly in terms of thefollowing-response of precocial birds (filial imprinting,e.g. Gottlieb 1971) and the development of sexual prefer-ences (sexual imprinting, e.g. ten Cate et al. 2006). The

ondence: B. T. Hansen, Department of Biology, Centre foral and Evolutionary Synthesis, University of Oslo, P.O. Boxndern, NO-0316 Oslo, Norway (email: b.t.hansen@bio.uio.no).

921472/08/$32.00/0 2007 The Association for the Stu

individuals (rival imprinting, Hansen & Slagsvold 2003).Learning by imprinting was originally thought to be

irreversible (Lorenz 1937). Early reports on the stability ofspecies preferences over time were anecdotal (reviewed inBateson 1966; Immelmann 1972a). In the first knownstudy to investigate experimentally the stability of matepreferences over several years, captive male zebra finches,Taeniopygia guttata, raised by Bengalese finch, Lonchurastriata, parents in the laboratory preferred to mate withBengalese finch females over several breeding attempts,even after extensive experience with conspecifics (Immel-mann 1972b).

More recent laboratory experiments on the zebra finch,however, have shown that mate preferences may bemalleable until the experience of first courtship. Birdsraised by heterospecific foster parents develop a preferencefor individuals of their foster species if they also

dy of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

mailto:b.t.hansen@bio.uio.no

ANIMAL BEHAVIOUR, 75, 3922

experience their first courtship with individuals of thatfoster species, but if such cross-fostered birds are exposedto conspecifics during first courtship or breeding, theymay shift their initial preference towards conspecifics(Bischof & Clayton 1991; Immelmann et al. 1991; Kruijt& Meeuwissen 1991; see also Kruijt & Meeuwissen 1993;Oetting et al. 1995; Oetting & Bischof 1996). These find-ings have been corroborated by studies of the zebra finchforebrain, where physical changes accompany the earlyexperiences as well as the experiences during first court-ship (reviewed in Bischof 2003). Thus sexual imprintingappears to be accomplished in two stages.

We have interspecifically cross-fostered wild great tits,Parus major, and blue tits, Cyanistes caeruleus, over severalyears and established that their species recognition isinfluenced by cross-fostering in terms of both mate prefer-ences (Slagsvold et al. 2002) and recognition of same-sexrivals (Hansen & Slagsvold 2003) in the field. In the pres-ent study we aimed to investigate the stability of this ac-quired species identity by comparing how the aggressivebehaviour of cross-fostered and control tits may changewith age. To our knowledge, the stability of imprintinghas never before been experimentally investigated in thewild. Great tits and blue tits differ in appearance and be-haviour, but have similar feeding and habitat preferencesand form mixed-species flocks outside the breeding season(e.g. Hinde 1952). Interspecific and intraspecific interac-tions are hence very common among these social tits.

Interspecifically cross-fostered birds may shift their pref-erence towards conspecifics if they possess some inherentown-species bias (Immelmann 1972a; Sonnemann &Sjolander 1977; Immelmann & Suomi 1981; Bischof &Clayton 1991). Also, cross-fostered birds might havelearned from interacting with conspecifics and heterospe-cifics 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 containingsome 450 nestboxes at Dli, near Oslo, Norway. Greattits and blue tits have been interspecifically cross-fosteredhere since 1995 (i.e. researchers have artificially trans-ferred eggs between nests of these two species). Cross-fostered individuals thrive in the nests of their hosts, buttheir adult behaviour differs from that of controls of theirown species (Slagsvold et al. 2002; Hansen & Slagsvold2003). We keep track of the local great tit and blue tit pop-ulations through individual colour banding of recruits.Nearly all great tits and blue tits breeding in the studyarea use the provided nestboxes.

We assigned birds to two treatment groups. (1) Controlbirds were unmanipulated and were raised by unmanip-ulated parents. (2) Cross-fostered birds were raised byunmanipulated heterospecific parents (great tit fosterparents for blue tit chicks and vice versa). For a more

detailed account of the general field procedures, see Slags-vold et al. (2002).

Cage Experiment

To determine aggressive responses, we exposed focalbirds to simulated territorial intrusions during the breed-ing season in 1999e2006. We sequentially presented focalbirds with a live, caged great tit or blue tit near theirnestbox between the onset of nest building and the startof incubation (1.1 4.8, mean SD, days after laying ofthe first egg). Focal and stimulus birds were always ofthe same sex. We allowed at least 1 h between the two tri-als, and we randomized the order of presentation. Werecorded the response of the focal bird as the time spentwithin 2 m of the cage during a 5-min trial. Close proxim-ity to the simulated intruder is most often accompaniedby clearly aggressive behaviour in terms of posture, chaseflights, etc. Thus, 64.5 36.9% of the time spent within2 m of the cage was spent in physical contact with thecage. We began trials immediately after the observer con-firmed that the resident focal bird was aware of the cagedintruder, with the criteria that the focal bird had an unob-structed view to the stimulus bird and had its attentiondirected towards the cage.

To ensure that stimulus birds (N 110) were unfamiliarto focal birds, they were caught outside the nestbox plot.While in captivity, we supplied them with meal wormsand water ad libitum. To balance the evils of keepinga large number of birds captive and engaging in stimuluspseudoreplication, we used most stimulus birds twicewithin each treatment group (1.7 0.9). We held stimulusbirds captive for 3.3 2.9 days and released them at thesite of capture. During trials, stimulus birds apparentlyavoided the response bird, at least when the latter perchedon the cage. Physical contact between the birds was hin-dered by the cage, as well as by the movements of thestimulus bird. We have never observed a stimulus bird tobe injured as a consequence of the experimental trials.None of the stimulus birds died in captivity. The reproduc-tion of stimulus birds could be negatively affected becausemost were territorial at capture. Potential effects includedelayed reproduction, displacement from their originalterritory and disruption of pair bonds. Stimulus birdswere caught before the initiation of reproduction (whileroosting in empty nestboxes), during nest building or dur-ing the early stages of egg laying (in mist nets). In this partof Norway, initiation of egg laying extends to the middleof June for both species of tits, while the terminationdate for our experiment was 19 May 6.6 days. Althoughwe did not have the capacity to monitor stimulus birdsafter release, we subsequently observed several breeding.For more details regarding the cage experiments andethical issues relating to the cross-fostering procedure,see Hansen & Slagsvold (2003).

Statistics

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

80

100

Con

spec

ific

agg

ress

ive

resp

onse

(%

)

(a)

(b)

80

60

40

20

0

100

1 2 3 4 5 6

HANSEN ET AL.: STABILITY OF LEARNED SPECIES RECOGNITION 923

great tits, 66 cross-fostered great tits), of which 254individuals were trialled in one breeding season only,and 58 individuals were trialled in at least two breedingseasons (8 control blue tits, 22 cross-fostered blue tits, 13control great tits, 15 cross-fostered great tits). In total therewere 394 observations per model on the complete data set(Table 1).

We performed separate analyses for aggressive re-sponses towards conspecifics and heterospecifics anda ratio between the two types of stimuli. The responseratio was calculated as [response towards conspecifics/(response towards conspecifics response towardsheterospecifics)] 100. A response ratio of 50% thusmeans that the responses towards conspecifics and heter-ospecifics are equal, a higher ratio means that aggressiveresponses are stronger towards conspecifics than towardsheterospecifics and a lower ratio means the opposite.Birds that spent no time within 2 m of the cage in eitherof the two trials were given a response ratio of 50%.

To avoid pseudoreplicating the response of the sameindividuals trialled in several breeding seasons, we usedmixed models to analyse the potential change with age inaggressive response towards conspecifics and heterospe-cifics (Pinheiro & Bates 2000). Initial models were fittedwith fixed effects for species, sex, treatment, age and theinteractions species:age, sex:age, treatment:age, treat-ment:species, treatment:species:age (entered in that order)and with random effect for individual. Initial models werereduced by backwards elimination. Models were fittedwith both equal and unequal variances between factorlevels and with random effects for intercept only and forintercept and slope. Alternative models were comparedin likelihood-ratio tests with maximum likelihood fits,and the most parsimonious model was in each case se-lected. However, the interaction between treatment andage was always retained in the model whether or not itimproved model fit. Model parameters were estimated byrestricted maximum likelihood. Alternative hypotheseswere not directional, and the a level was 0.05. Statisticalmodelling was performed with R 2.4.0 (R DevelopmentCore Team 2006).

60

40

20

RESULTS

The aggressive response towards conspecific intruders wasstronger in blue tits than in great tits (F1,308 160.21,P < 0.0001) and stronger in controls than in cross-fosteredbirds (F1,308 7.35, P 0.007), but the treatment effectdiffered between species (F1,308 24.98, P < 0.0001). In

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

Age (years)

1 2 3 4 5 6

Great tit control 46 26 10 10 2 0Great tit cross-fostered 45 22 14 4 3 1Blue tit control 63 21 8 3 1 0Blue tit cross-fostered 68 26 16 5 0 0

blue tits, controls and cross-fostered birds responded sim-ilarly, while great tit controls responded more stronglythan cross-fostered birds towards conspecific intruders(Fig. 1). Furthermore, there was a significant decrease inaggressive response with increasing age (F1,78 13.08,P 0.001). The effect of age tended to differ betweentreatments (F1,78 2.66, P 0.11), and there tended tobe a species difference in the interaction between ageand treatment (F2,78 2.65, P 0.08). Interaction plots(Fig. 1) suggest that in blue tits the reduced aggressiveresponse with age towards conspecifics did not differbetween the treatments, while in great tits controls

0

1 2 3 4 5Age (years)

Figure 1. Change in mean SE aggressive response with age to-wards 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 of5 min spent within 2 m of a caged conspecific intruder. Number of

observations is given in Table 1.

ANIMAL BEHAVIOUR, 75, 3924

reduced their response with age to a greater extent thandid cross-fostered birds.

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

80

60

40

20

0

100

1 62 3 4 5

80

60

40

20

0

100

Het

eros

pec

ific

agg

ress

ive

resp

onse

(%

)

1 2 3 4 5Age (years)

(a)

(b)

Figure 2. Change in mean SE aggressive response with age to-wards 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 of5 min spent within 2 m of a caged heterospecific intruder. Number

of observations is given in Table 1.

heterospecifics further showed a decrease in responsewith increasing age (F1,80 15.64, P 0.0002; Fig. 2). Im-portantly, the effect of age was similar for controls andcross-fostered birds (F1,80 0.98, P 0.33).

The response towards conspecifics relative to thattowards heterospecifics (i.e. the response ratio) differedbetween the species (F1,309 26.65, P < 0.0001), with bluetits responding more towards conspecifics than heterospe-cifics compared to great tits. Controls responded relativelymore towards conspecifics than towards heterospecifics incomparison with cross-fostered birds (F1,309 206.11,P < 0.0001). However, there was no effect of age on the re-sponse ratio (F1,80 0.47, P 0.50) because the rates ofdecline in aggressive response with age were similar inthe responses towards both conspecifics and heterospe-cifics. Furthermore, there was no interaction betweentreatment and age (F1,80 0.28, P 0.60); hence bothcontrols and cross-fostered birds showed a similar lack ofeffect of age on the response towards conspecifics relativeto the response towards heterospecifics (Fig. 3).

Because the cross-fostered birds responses to hetero-specifics seem similar to the controls responses to con-specifics, comparing the aggressive response towardsconspecifics for controls and the aggressive responsetowards heterospecifics for cross-fostered birds is justified.The model shows that blue tits responded more aggres-sively than great tits (F1,309 59.23, P < 0.0001) and thatcontrols responded somewhat more than cross-fosteredbirds (F1,309 5.88, P 0.02). Again, aggression wanedwith age (F1,79 25.75, P < 0.0001), and this happenedat a faster rate in great tits than in blue tits (F1,79 7.07,P 0.01). Note, however, that there was no differencebetween controls and cross-fostered birds in the rate ofdeclining aggressive response with age (F1,79 0.22,P 0.64). Hence, cross-fostered birds did not respondless towards heterospecifics with increasing age than didcontrols towards conspecifics.

We also performed separate analyses on the 58 birdstrialled in several breeding seasons (Tables A1 and A2 inthe Appendix). These analyses confirmed our mainfindings.

DISCUSSION

Cross-fostered birds responded more to heterospecificsthan did controls, and cross-fostered great tits respondedless towards conspecifics than did controls, while bothcross-fostered and control blue tits responded highlyaggressively towards conspecifics. These results confirmthose from a previous study with a smaller sample(Hansen & Slagsvold 2003). We show that these differ-ences between controls and cross-fostered birds are quiterobust with increasing age. The aggressive response de-creases with age at a similar rate in both treatments andin both species and in response towards conspecifics aswell as heterospecifics. Hence, although the absolute levelof aggression changes with age, differences between con-trols and cross-fostered birds persist. Consequently, theresponse towards conspecifics relative to that towards het-erospecifics appears unaffected by age for both treatments.

80

60

40

20

0

100

1 62 3 4 5

80

60

40

20

0

100

Agg

ress

ive

resp

onse

rat

io (

%)

1 2 3 4 5Age (years)

(b)

(a)

Figure 3. Change in mean SE aggressive response ratio with agetowards conspecific relative to heterospecific intruders for cross-

fostered (C, solid regression line) and control (O, dashed regression

line) (a) great tits and (b) blue tits. Aggressive response ratio is mea-sured 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.

HANSEN ET AL.: STABILITY OF LEARNED SPECIES RECOGNITION 925

Hence, interspecifically cross-fostered great tits and bluetits become imprinted on their foster species, and thislearned species recognition is not shifted towards conspe-cifics during adulthood. The original imprinting thusseems to persist throughout life, even though the cross-fostered birds have had unlimited opportunities to inter-act with both conspecifics and heterospecifics.

Blue tits are more responsive than great tits to thepresentation of caged intruders. One of the models alsoindicates that the negative effect of age on aggression may

be stronger in great tits than in blue tits. Blue tits areknown for their fiery temper (Colquhoun 1942), and ourgeneral impression is that great tits are somewhat moreshy than blue tits. This may explain the observed speciesdifferences in aggressive response. Another general find-ing is that the aggressive response declines with age. Wethink that experienced birds improve in identifying realthreats and may respond less to a caged intruder presentedby a human. Furthermore, older birds may have higherstatus and thus deem a fight unnecessary to defend theirinterests, or they may simply have less fighting abilitythan younger birds. It is also possible that shy birds livelonger and that we observe a population increase in shybirds rather than an age-effect per se. The birds used inseveral years represent a sample of relatively old birds.Hence, if shyness is important, we expect no age-effectand a low aggressive response as yearlings for these birds.This is not the case, which indicates that we are in factobserving an effect of age.

The aggressiveness of great tit controls towards conspe-cifics decreases at a faster rate than is the case for cross-fostered birds. We do not know what causes thisdifference. However, control yearlings have a high re-sponse while cross-fostered yearlings have a low responsetowards conspecifics. Control great tits thus have a greaterscope for a decrease in aggressiveness with age than docross-fostered great tits.

Evidence from studies on captive birds indicates thatmate preferences may change with experience until theevent of first courtship/mate choice (Bossema & Kruijt1982; Kruijt et al. 1982; ten Cate et al. 1984; Bischof &Clayton 1991; Immelmann et al. 1991; Kruijt & Meeuwis-sen 1991, 1993; Oetting et al. 1995; Oetting & Bischof1996). The results on the potential effects of experiencebeyond first 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), whilethe preferences of cross-fostered females may shift towardsconspecifics with increasing age (ten Cate & Mug 1984).From these laboratory studies one can conclude that theacquired preferences of zebra finches cross-fostered toBengalese finches are unstable until first courtship, but re-main quite stable thereafter, and that there might be somescope for change even after first courtship, given certainexperimental conditions.

Tits breeding in our study area encounter nonfamiliarconspecifics and heterospecifics almost immediately afterfledging, because the breeding populations are dense(about one tit pair/ha) and most broods fledge withina week of each other. These tits are social throughout lifeand form mixed-species flocks during late summer, au-tumn and winter (Perrins 1979). Aggressive interactionsover food, both intra- and interspecifically, are common.The larger great tits are dominant over blue tits, and malesare dominant over females (Hansen & Slagsvold 2004). Insuch a system species recognition is not likely to be con-solidated during first courtship, because fledglings arenot likely to experience courtship until the followingbreeding season, and they must be able to distinguish be-tween species as well as sexes in the many interactions

ANIMAL BEHAVIOUR, 75, 3926

they are bound to experience during their first summer,autumn and winter. Repeated errors in this respect willprobably be costly. Hence, stable species recognition basedon the initial imprinting on parental characteristicsshould be established early in the life of these tits. We sug-gest that if courtship behaviour influences mate recogni-tion under natural circumstances in social species suchas tits, the formation of the species recognition that isfunctional during the nonbreeding season must be sepa-rate from the species recognition confirmed throughmate choice (see also Bischof 2003).

Interestingly, the outcome of the misdirected aggressiondoes not seem to influence species recognition. In winter,cross-fostered great tits generally win aggressive interac-tions over food against blue tits, while cross-fostered bluetits lose against great tits (Hansen & Slagsvold 2004). Nev-ertheless, this study shows that cross-fostered birds ofboth species retain the mistaken species recognition;hence blue tits do not become any wiser from losingthan great tits become from winning.

Several authors have observed that interspecificallycross-fostered individuals prefer conspecifics and haveinterpreted this phenomenon as an own-species bias (e.g.Klint 1975). However, an alternative explanation for someof these findings is that the cross-fostered individuals maynot have been able to choose freely, but instead have re-sponded to the individuals courting them most intensely,which in most cases will be conspecifics (e.g. Bossema &Kruijt 1982). This is likely to apply to the tits in the presentstudy as well. Sometimes a cross-fostered great tit anda cross-fostered blue tit of opposite sex meet and form a het-erospecific pair (Slagsvold et al. 2002). However, most birds,irrespective of treatment, are more likely to be courted byconspecifics because unmanipulated birds outnumbercross-fostered birds. Judging from the aggressive responsetowards intruders of both species, courtship experienceswith conspecifics have not corrected the species recogni-tion of cross-fostered birds, because even those breedingwith conspecifics show the same pattern of aggressive re-sponse as other cross-fostered birds (Hansen et al. 2007).

In conclusion, acquired species recognition of wild greattits and blue tits seems to be irreversible once it has beenestablished. Extensive experience from natural interac-tions with conspecifics and heterospecifics throughout lifedoes not seem to affect species recognition. The vastmajority of studies on imprinting have been performedin the laboratory under extremely unnatural conditions.This field study enhances understanding of the naturalfunction of this learning process. This is also the first timethat the stability of imprinted species recognition hasbeen investigated in terms of same-sex species recogni-tion. Surprisingly, the development of rival recognitionhas been almost completely overlooked in previousstudies on imprinting.

Acknowledgments

We thank everyone who helped us in the field, theVestgard 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 themanuscript. The Research Council of Norway fundedgrants for L.E.J. and B.T.H. The study complied withNorwegian law and was conducted under licences fromthe Directorate for Nature Management and the NationalAnimal Research Authority in Norway.

References

Bateson, P. P. G. 1966. The characteristics and context of imprint-ing. Biological Reviews, 41, 177e220.

Bischof, H. J. 2003. Neural mechanisms of sexual imprinting. AnimalBiology, 53, 89e112.

Bischof, H. J. & Clayton, N. 1991. Stabilization of sexual preferencesby sexual experience in male zebra finches Taeniopygia guttata

castanotis. Behaviour, 118, 144e155.

Bossema, I. & Kruijt, J. P. 1982. Male activity and female mate ac-ceptance in the mallard (Anas platyrhynchos). Behaviour, 79,313e324.

Colquhoun, M. K. 1942. Notes on the social behaviour of blue tits.British Birds, 35, 234e240.

Gottlieb, G. 1971. Development of Species Identification in Birds.Chicago: University of Chicago Press.

Hansen, B. T. & Slagsvold, T. 2003. Rival imprinting: interspecifi-cally cross-fostered tits defend their territories against heterospe-cific intruders. Animal Behaviour, 65, 1117e1123.

Hansen, B. T. & Slagsvold, T. 2004. Early learning affects socialdominance: interspecifically cross-fostered tits become subdomi-

nant. Behavioral Ecology, 15, 262e268.

Hansen, B. T., Johannessen, L. E. & Slagsvold, T. 2007. No culturaltransmission of species recognition between parents and offspring

in free-living great tits and blue tits. Behavioral Ecology and Socio-

biology, 61, 1203e1209.

Hess, E. H. 1973. Imprinting. Early Experience and the DevelopmentalPsychobiology of Attachment. New York: Van Nostrand Rheinhold.

Hinde, R. A. 1952. The behaviour of the great tit (Parus major) andsome other related species. Behaviour Supplement, 2.

Immelmann, K. 1972a. Sexual and other long-term aspects ofimprinting in birds and other species. Advances in the Study ofBehavior, 4, 147e174.

Immelmann, K. 1972b. The influence of early experience upon thedevelopment of social behaviour in estrildine finches. In: Proceed-

ings of the XV International Ornithological Congress, Haag 1970,

pp. 316e338.

Immelmann, K. & Suomi, S. J. 1981. Sensitive phases in develop-ment. In: Behavioral Development (Ed. by K. Immelmann, G. W.

Barlow, L. Petrinovich & M. Main), pp. 395e431. Cambridge:Cambridge University Press.

Immelmann, K., Prove, R., Lassek, R. & Bischof, H. J. 1991.Influence of adult courtship experience on the development of

sexual preferences in zebra finch males. Animal Behaviour, 42,83e89.

Kendrick, K. M., Hinton, M. R., Atkins, K., Haupt, M. A. & Skinner,J. D. 1998. Mothers determine sexual preferences. Nature, 395,229e230.

Klint, T. 1975. Sexual imprinting in the context of species recognitionin female mallards. Zeitschrift fur Tierpsychologie, 38, 385e392.

Kruijt, J. P. & Meeuwissen, G. B. 1991. Sexual preferences of malezebra finches: effects of early and adult experience. Animal Behav-

iour, 42, 91e102.

Kruijt, J. P. & Meeuwissen, G. B. 1993. Consolidation and modifi-cation of sexual preferences in adult male zebra finches. Nether-lands Journal of Zoology, 43, 68e79.

Appendix

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

df F P

Intercept 1,79 380.39