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Animal Behaviour 80 (2010) 189e195

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From preferential response to parental calls to sex-specific response to conspecific calls in juvenile zebra finches Hervé Mulard*, Clémentine Vignal, Lise Pelletier, Alain Blanc, Nicolas Mathevon Université de Saint-Etienne, Equipe de Neuro-Ethologie Sensorielle, ENES/CNPS CNRS UMR 8195, France Centre National de la Recherche Scientifique, ENES/CNPS, UMR 8195

a r t i c l e i n f o Article history: Received 9 May 2009 Initial acceptance 9 June 2009 Final acceptance 12 April 2010 Available online 8 June 2010 MS. number: 09-00306R Keywords: acoustic communication individual signature long-term memory parenteoffspring recognition postfledging care sex difference Taeniopygia guttata vocal recognition zebra finch

In birds, parenteoffspring recognition is crucial for directed parental care, and is often based on acoustic cues. The strength and the time of onset of this recognition process depend on ecological factors that constrain parental care. For instance, parenteoffspring recognition generally appears earlier in nidifugous than in nidicolous species. We investigated whether fledglings in a nidicolous species, the zebra finch, Taeniopygia guttata, recognize their parents and the fate of this recognition process once the parents had stopped their food provisioning. Zebra finches are gregarious passerines that provide parental care to chicks up to 20 days after fledging. In playback experiments, fledglings preferentially responded to parental calls over other adult calls and thus recognized both their father’s and mother’s distance calls. However, at 2 months, motivation to respond to parental and other adult calls became sex specific, with sons no longer reacting preferentially to their father’s calls, whereas daughters did. This pattern may be linked to the development of sexual traits and mate-searching behaviours. The persistence of parent recognition at the age of pair formation may also be of critical importance during mate choice. ! 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

In birds, recognition between parents and offspring can be of crucial importance during the parental care period, especially for parents to avoid misdirected parental care and limit infanticide. In general, acoustic channel recognition is bidirectional: offspring are able to identify their parents’ vocalizations and parents recognize their chicks’ begging calls (e.g. in penguins: Aubin & Jouventin 2002b; Aubin et al. 2004). However, parenteoffspring recognition is not mandatory and seems to develop only if and when needed. In nidicolous species for instance, parenteoffspring recognition is thought to be poorly developed since the nest functions as a ‘meeting place’, limiting the risks of confusion between kin and nonkin (e.g. Mathevon et al. 2003). Efficient parenteoffspring recognition, assumed to appear only once chicks fledge and therefore are mobile, thus allows for the maintenance of directed parental provisioning (e.g. Barg & Mumme 1994; Leonard et al. 1997; Insley et al. 2003). In several species of passerines, brood division, where each parent takes care of specific fledglings, is linked to a precise parenteoffspring recognition process (Slagsvold

* Correspondence and present address: H. Mulard, Université de Saint-Etienne, Equipe de Neuro-Ethologie Sensorielle ENES/CNPS, CNRS UMR 8195, 23 rue Michelon, 42023 Saint-Etienne cedex 2, France. E-mail address: [email protected] (H. Mulard).

1997; Green & Cockburn 2001; Lessells 2002; Leedman & Magrath 2003; Draganoiu et al. 2005). In colonial species where juveniles gather in crèches and it may be difficult for parents to find their offspring, individual recognition between parents and young is usually highly efficient (e.g. in passerines: Falls 1982; Stoddard & Beecher 1983; Medvin & Beecher 1986; Beecher 1990; Leonard et al. 1997; in penguins: Aubin & Jouventin 2002b). If the existence or the onset of parenteoffspring vocal recognition is constrained by ecological factors linked to parental care, what is the fate of this recognition process once the parents have stopped their provisioning and offspring are able to feed by themselves? Owing to an imprinting-like phenomenon, adult birds show a preference for the sexual characteristics of their parents, for example their father’s song, in adulthood (Miller 1979; Clayton 1988; Adret 1993; Riebel 2000). However, these signals are not those that usually support parenteoffspring recognition in the context of directed parental care. In this situation, parents and chicks generally utter simple contact calls, lacking the usual complicated embellishment of sexual vocal signals. To the best of our knowledge, no study has investigated whether after independence young songbirds still target their behavioural response towards parenteoffspring meeting calls. It is likely that one of the following three situations may occur: (1) a preferential response remains: young birds still respond preferentially to their parents’

0003-3472/$38.00 ! 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.04.011

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signals as a by-product of long-term memory of parental vocalizations; (2) a disappearing response: young birds no longer prefer their parents’ signals because they are no longer functional; and (3) a subtle pattern of modification: the preference towards parents’ signals persists but undergoes modification linked to the transition to adulthood where acoustic signals represent cues to manage social relationships with nonparents. The aim of our study was to investigate this question in the zebra finch, Taeniopygia guttata, a gregarious passerine of the Estrildidae family, in which parental care occurs up to 20 days after fledging (Zann 1996). During this period, fledglings may group in crèches, increasing the risk of confusion for parents identifying offspring. The vocal repertoire of adult zebra finches includes the male song, a complicated arrangement of notes used for female attraction and pair bond maintenance, and several one-note calls uttered by both males and females (Zann 1996). The distance call of both sexes is known to support individual recognition between partners. Both males and females distinguish the distance call of their sexual partner from those of other individuals (Vignal et al. 2004, 2008a, b; Zann 1996). Parental distance calls are also used in the context of parenteoffspring meeting during the postfledging period (Zann 1996), but the effectiveness of parenteoffspring recognition has received very little attention. Although zebra finches can recognize their own chicks on the basis of their begging calls (Levrero et al. 2009), it is unknown whether offspring rely on parental distance calls to recognize their parents among the other adults of the colony. Here, we assessed recognition of parental distance calls by fledglings using playback experiments. Then, we studied how this preferential response to parental calls over other adult calls varies between fledging and 2 months of age. At this latter stage, young are fully independent and may form pairs (Zann 1996), potentially leading to differences in motivation to respond to vocalizations according to the sex of the young and the broadcasting adult’s sex and identity. METHODS Housing Conditions Pairs of zebra finches were bred in individual cages (40 ! 40 cm and 25 cm high), equipped with a commercially made woven nest and two perches, from May 2007 to July 2008. Food (Tropical Finches Prestige seeds and Orlux eggfood, Versele-Laga NV, Deinze, Belgium), nest materials (paper and sprigs) and water were provided ad libitum. All breeding cages were in the same room (light conditions: 14:10 h light:dark; temperature from 23 to 28" C; humidity ca. 40e60%). Birds were therefore able to hear each other. Twice a week, the position of the cages in the room was modified, enabling birds to see others. Thus, all birds in the room can be considered as familiar to each other. In total, we used 22 mating pairs which reared 54 chicks (23 males, 31 females, one to five chicks per brood). These pairs were not established simultaneously, and consequently breeding was asynchronous between pairs (eggs hatching between May 2007 and April 2008). Experiments were done under the authorization of the Université de Saint-Etienne and of the Veterinary Department of the Loire Prefecture. Bird housing was licensed by the Veterinary Department of the Loire Prefecture. Recordings Distance calls (Zann 1996) of adults were recorded at about 30 cm from the calling bird in an acoustic chamber (Silence Box, Tip-Top Wood, Saint-Etienne, France) using a Sennheiser MD42 microphone connected to a Marantz PMD670 recorder. During the recording sessions, birds were placed alone in a cage, but two to

four other cages of familiar paired individuals were present in the room to promote bird reactivity (Vignal et al. 2004). Playback Experiments To test for reaction to familiar calls, we placed fledglings and juveniles in a cage (97 ! 57 cm and 57 cm high) equipped with three perches 30 cm from each other, with food and water available ad libitum. Each side of the cage was equipped with a loudspeaker (Teac LS-35 M), connected to a Yamaha AX397 amplifier. Four cages of familiar paired individuals, different from those used as playback stimuli, were placed in the test room at about 2 m from the test cage to promote bird reactivity (Vignal et al. 2004). At the time of the test, fledglings were a mean # SD of 21.9 # 2.6 days old (18e27 days; the 50 fledglings were tested less than a week after their actual fledging occurring between day 16 and 22 posthatch), and the juveniles were 56.4 # 2.4 days old (52e65 days; 38 juveniles tested). We did not test juveniles earlier than 52 days of age, to be sure that they were fully independent (parental care may occur until 40 days posthatching, Zann 1996). Four chicks were not tested at fledging, and 16 were not tested at 2 months (either because they died or because they were part of another experiment at this stage). Juveniles were sexed when plumage started to be dimorphic (between 6 and 8 weeks). From fledging to the time of the test, all juveniles remained with their parents in the same cage. Each bird experienced two playback sessions in random order (one session with male stimuli, one session with female stimuli), separated by at least 5e10 min. Each playback session consisted of six series of five calls. Within each series, each call was separated from the next one by 2 s, mimicking a natural sequence (H. Mulard, personal observation), and series were separated by at least 40 s, enough time for the bird to regain a basal activity level. Among these six series, three contained different calls from one parent and three contained different calls from a given familiar adult of the same sex. Each bird was thus tested three times for a given origin of call. Familiar adults used to create nonparent stimuli were randomly chosen for each session among the adults nesting in neighbouring cages. Series were played from either loudspeaker (left or right). Series order and playing loudspeaker (each session: three randomly chosen series played on the right, three on the left) were randomly chosen before the session. We used the intensity of calls given by familiar individuals placed in the test room as an audience to promote subjects’ reactivity (see above) as a sound intensity reference for the playback. The root mean square (RMS) sound pressure of the stimuli was set at half the RMS value of the audience’s calls using Goldwave version 5.20 software (GoldWave Inc., St Johns, NL, Canada). The behaviour of the test bird was monitored using an IP DLINK DSC 900 camera. Evoked calls were also recorded using the

Table 1 Number of chicks reacting to each type of broadcast call Stage of test Fledging No. of chicks No. of FþM No. of broods

Reacting to male calls

Reacting to female calls

Reacting to both male and female calls

No reaction to any call

30 17Fþ13M 16

25 12Fþ13M 15

19 11Fþ8M 13

14 10Fþ4M 10

23 13Fþ10M 12

14 9Fþ5M 9

10 5Fþ5M 7

Two months old No. of chicks 19 No. of FþM 13Fþ6M No. of broods 11

For fledglings, N ¼ 50, 28Fþ22M, from 22 broods; for 2-month-old birds, N ¼ 38, 22Fþ16M, from 18 broods. F: females; M: males.

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apparatus described in the previous section. For 25 s following the playback of the first call of each of the six playback series, we measured the number of calls (distance calls for juveniles, long-tonal or begging calls for fledglings) given by the bird and the latency to the first call, that is, the time before the test bird’s first call. Latency was calculated from the beginning of the first call of each series. When the test bird did not call during the 25 s, latency was arbitrarily fixed at 26 s.

factors were individual identity (34 levels) and brood identity (17 levels). The interaction effects considered were nature of the stimulus*stage, sex of the stimulus*stage and sex of the chick*stage. All statistical analyses were performed with R software (R Development Core Team 2007). We used the lmer() function of the lme4 package (Bates 2005; Bates & Sarkar 2007) which allowed us to define multiple distinct random factors. To obtain P values, we used Markov chain Monte Carlo (MCMC) simulations (pvals.fnc() in R, Baayen et al. 2008). The degree of freedom used for the t distribution by the MCMC simulations is an upper bound: the number of observations minus the number of fixed-effects parameters.

Data Analysis and Statistics To test the effect of the playback stimuli on the behavioural response of chicks (number of calls and latency to first call), we used a linear mixed model (LMM). This model was first applied to the data obtained at the fledging stage, then to the data obtained at 2 months of age. We used an LMM with the nature of the stimulus (two levels: parent versus familiar), the sex of the stimulus (two levels: female versus male calls), the order of playback presentations (six levels), the sex of the chicks (two levels) and the age of the chick (continuous covariate) as fixed factors. The random factors were individual identity (50 levels at fledging stage, 38 levels at 2-months stage) and brood identity (22 levels at fledging stage, 18 levels at 2-months stage). The interaction effects considered were sex of the stimulus*nature of the stimulus, order*nature of the stimulus, sex of the chick*nature of the stimulus, order*sex of the stimulus, sex of the chick*sex of the stimulus. At 2 months of age, the LMM also considered the interaction sex of the stimulus*nature of the stimulus*sex of the chick. To test for changes in chicks’ reactivity between fledging and 2 months of age, we used an LMM with the stage (two levels: fledging versus 2 months), the nature of the stimulus (two levels: parent versus familiar), the sex of the stimulus (two levels: female versus male calls), the order of playback presentations (six levels) and the sex of the chicks (two levels) as fixed factors. The random

RESULTS Fledgling Responses Fifty fledglings (Table 1) were tested for their response to four different types of call (mother, father, familiar female, familiar male). Among the 25 fledglings that reacted to female calls (Table 1), 11 (five females, six males) reacted both to the mother and the familiar female, and 14 (seven females, seven males) reacted only to the mother. None of the fledglings reacted only to the nonparent familiar female calls, indicating that fledglings reacted preferentially to their mother’s calls. Among the 30 fledglings that reacted to male calls (Table 1), 12 (five females, seven males) reacted both to the father and the nonparent familiar male and 18 (12 females, six males) reacted only to the father. Once again, none of the fledglings reacted only to familiar male calls, indicating that fledglings reacted preferentially to their father’s calls. Number of calls Fledglings responded more to the calls of their father and mother than to nonparent familiar calls (significant interaction: sex of the stimulus*nature of the stimulus; Tables 2, 3; paired t test with Bonferroni correction: female parent versus familiar female: P ¼ 0.046; male parent versus familiar male: P < 0.001; Fig. 1). Furthermore, whereas vocal response to male and female familiar calls did not differ (P ¼ 0.244), fledglings answered with more calls to their father than to their mother (P < 0.001). The sex of the fledgling did not influence the response to the playback, nor did the order of presentation or the continuous variable age (Tables 2, 3).

Table 2 Statistical analysis of the effect of playback stimuli on behavioural response (number of calls and latency to first call) of fledglings: random effects Random effect

Individual Brood identity Residual

Number of calls

Latency to first call

Variance

SD

Variance

SD

14.3 2.4 40.1

3.8 1.5 6.3

29.3 13.1 70.7

5.4 3.6 8.4

Latency to first call Fledglings reacted faster to the calls of their parents than to nonparent familiar calls (significant effect of the nature of the stimulus; Tables 2, 3, Fig. 1). Furthermore, whereas latency to first

Linear mixed models were performed using the lmer() function of the lme4 package in R software.

Table 3 Statistical analysis of the effect of playback stimuli on behavioural response (number of calls and latency to first call) of fledglings: fixed effects Fixed effects

Intercept Order SS Nature Age SC SS*Nature Order*Nature SC*Nature Order*SS SC*SS

Number of calls

Latency to first call

Estimate

SE

t

P

Estimate

SE

t

P

&7.3 &0.12 1.9 2.3 0.36 1.1 2.8 0.040 &0.15 0.24 &2.0

6.1 0.27 1.3 1.4 0.28 1.5 1.0 0.32 1.0 0.31 1.0

&1.2 &0.44 1.4 1.7 1.3 0.7 2.7 0.13 &0.15 0.80 &1.9

0.23 0.66 0.17 0.098 0.19 0.47 0.008 0.90 0.88 0.42 0.058

32.9 &0.041 &2.3 &7.3 &0.41 &3.2 &3.1 0.47 1.2 0.015 2.9

10.0 0.36 1.8 1.9 0.45 2.2 1.4 0.42 1.4 0.41 1.4

3.3 &0.12 &1.3 &3.9 &0.90 &1.5 &2.2 1.1 0.86 0.036 2.1

0.0011 0.91 0.20 0.0001 0.37 0.14 0.026 0.27 0.39 0.97 0.039

Linear mixed models were performed using the lmer() function of the lme4 package in R software. P values were obtained using Markov chain Monte Carlo simulations (pvals. fnc() function). Significant P values are displayed in bold. Order: order of playback presentations; SS: sex of the stimulus (male versus female); nature: nature of the stimulus (parent versus familiar adult); age: age of the chick; SC: sex of the chick.

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Figure 1. Reactions of fledglings towards the different types of call. (a) Mean number of calls (long-tonal or begging) and (b) mean latency to first call in response to calls of a familiar male or the father. (c) Mean number of calls (long-tonal or begging) and (d) mean latency to first call in response to calls of a familiar female or the mother. Only fledglings that reacted to at least one of the two types of call (parent versus familiar) for each adult sex are represented (N ¼ 30 towards males, N ¼ 25 towards females). Each point represents one individual. See the text for test values.

call in response to male and female familiar calls did not differ (significant interaction: sex of the stimulus*nature of the stimulus; Tables 2, 3; paired t test with Bonferroni correction: P ¼ 1), fledglings responded more rapidly to their father than to their mother (P ¼ 0.005). The order of presentation and the age of the chick did not influence the latency to first call (Tables 2, 3). In contrast, the sex of the chick showed a significant interaction with the sex of the stimulus (Tables 2, 3): female fledglings reacted faster to male stimuli than to female stimuli (paired t test with Bonferroni correction: P ¼ 0.011). To summarize, the parents’ calls evoked more calls and faster reactions than nonparent calls in chicks around fledging age.

Fledglings responded with more calls and more rapidly to their father than to their mother. Female fledglings showed faster responses to male stimuli than to female stimuli.

Juvenile Responses and Sex Differences Thirty-eight juveniles (Table 1) were tested for their response to the four different types of call. Number of calls Juveniles responded more to the calls of their father and mother than to nonparent familiar male calls (significant interaction: sex of the stimulus*nature of the stimulus; Tables 4, 5; paired t test with Bonferroni correction: female parent versus familiar male: P ¼ 0.027; male parent versus familiar male: P ¼ 0.007; Fig. 2) but there was no difference in response to nonparent familiar female calls (P ¼ 1). The order of presentation and the age of the juvenile did not influence the number of calls (Tables 4, 5). In contrast, the sex of the juvenile showed a significant interaction with the sex of the stimulus and the nature of the stimulus (Tables 4, 5): daughters responded with more calls to their father than to the nonparent familiar male (paired t test with Bonferroni correction: P ¼ 0.001), whereas sons did not (P ¼ 1), and daughters responded with more calls to their father than sons did (P < 0.001).

Table 4 Statistical analysis of the effect of playback stimuli on behavioural response (number of calls and latency to first call) of 2-month-old juveniles: random effects Random effects

Individual Brood identity Residual

Number of calls

Latency to first call

Variance

SD

Variance

SD

3.4 6.1!10&17 5.0

1.8 7.8!10&9 2.2

46.4 0 70.8

6.8 0 8.4

Linear mixed models were performed using the lmer() function of the lme4 package in R software.

Table 5 Statistical analysis of the effect of playback stimuli on behavioural response (number of calls and latency to first call) of 2-month-old juveniles: fixed effects Fixed effects

Intercept Order SS Nature Age SC SS*Nature Order*Nature SC*Nature Order*SS SC*SS SS*Nature*SC

Number of calls

Latency to first call

Estimate

SE

t

P

Estimate

SE

t

P

7.1 0.036 &0.38 0.16 &0.099 &0.20 2.1 &0.053 0.71 &0.068 &0.29 2.5

7.8 0.11 0.56 0.57 0.14 0.75 0.53 0.12 0.58 0.12 0.59 0.84

0.91 0.34 &0.69 0.28 &0.71 &0.26 3.9 &0.43 1.2 &0.56 &0.50 &3.0

0.36 0.74 0.49 0.78 0.78 0.80 0.0001 0.67 0.22 0.58 0.62 0.003

&18.2 0.13 1.7 &3.7 0.66 &1.7 &5.0 0.63 &1.8 &0.16 3.2 6.7

28.7 0.40 2.1 2.1 0.51 2.8 2.0 0.46 2.2 0.46 2.2 3.2

&0.64 0.32 0.81 &1.7 1.3 &0.60 &2.5 1.4 &0.80 &0.35 1.4 2.1

0.52 0.75 0.42 0.081 0.20 0.55 0.014 0.17 0.43 0.73 0.15 0.040

Linear mixed models were performed using lmer() function of the lme4 package in R software. P values were obtained using Markov chain Monte Carlo simulations (pvals.fnc() function). Significant P values are displayed in bold. Fixed-effects variables are abbreviated as in Table 3.

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Latency to first call Juveniles reacted faster to the calls of their father and mother than to nonparent familiar male calls (significant interaction: sex of the stimulus*nature of the stimulus; Tables 4, 5; paired t test with Bonferroni correction: female parent versus familiar male: P ¼ 0.003: male parent versus familiar male: P ¼ 0.021; Fig. 2) but there was no difference in response to nonparent familiar female calls (P ¼ 0.8 and P ¼ 1). The order of presentation and the age of the juvenile did not influence the latency (Tables 4, 5). In contrast, the sex of the juvenile showed a significant interaction with the sex of the stimulus and the nature of the stimulus (Tables 4, 5): daughters responded faster to their father than to the nonparent familiar male (paired t test with Bonferroni correction: P ¼ 0.022), whereas sons did not (P ¼ 1), and daughters responded faster to their father than sons did (P ¼ 0.01). To summarize, the calls of the parents evoked more calls and faster reactions than nonparent male calls but there was no difference in response to nonparent female calls in juveniles around 2 months of age. Nevertheless, the difference in the number of evoked calls and the latency to first call between male parental calls and nonparent male calls was only significant in daughters, which responded more to their father than to nonparent males. Development of Juvenile Reactivity Thirty-four young birds (19 females and 15 males) belonging to 17 different broods were tested both at fledging and at 2 months old.

(a)

24

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Number of calls Juveniles at 2 months of age called less in response to the playback than fledglings (significant effect of stage; Tables 6, 7). Parental calls evoked less calling at 2 months than at fledging (significant interaction: nature of the stimulus*stage; paired t test with Bonferroni correction: P < 0.001). Male calls were less effective in stimulating calling at 2 months than at fledging (significant interaction: sex of the stimulus*stage; paired t test with Bonferroni correction: P < 0.001). Latency to first call Juveniles at 2 months of age reacted faster in response to the playback than fledglings (significant effect of stage; Tables 6, 7). Juveniles reacted faster to the calls of their parents than to nonparent familiar calls at 2 months as at fledging (significant interaction: nature of the stimulus*stage: paired t test with Bonferroni correction: familiar call versus parental call at fledging: P < 0.001; familiar call versus parental call at 2 months: P ¼ 0.004), but the latency of response to nonparent familiar calls decreased from fledging to 2 months (familiar call at fledging versus parental call at 2 months: P ¼ 0.022). In particular, latency of response to nonparent female calls decreased in both sexes from fledging to 2 months (significant interaction: sex of the stimulus*stage: paired t test with Bonferroni correction: P ¼ 0.016). To summarize, the preferential calling response to parental calls was attenuated from fledging to 2 months because of a decrease in calling evoked by the calls of the father and an increase in reactivity to nonparent calls, especially to nonparent female calls.

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Figure 2. Reactions of 2-month-old juveniles towards the different types of call. (aed) Males; (eeh) females. (a, e) Mean number of calls (long-tonal or begging) and (b, f) mean latency to first call in response to calls of a familiar male or the father. (c, g) Mean number of calls (long-tonal or begging) and (d, h) mean latency to first call in response to calls of a familiar female or the mother. Only fledglings that reacted to at least one of the two types of call (parent versus familiar) for each adult sex are represented (response to males: six males, 13 females; response to females: 10 males, 13 females). See the text for test values.

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DISCUSSION

another purpose later in life. Indeed, at 2 months, female juveniles still strongly reacted to their father’s calls, while the magnitude of the preferential response to parental calls decreased in both female and male juveniles from fledging to 2 months of age. At 2 months, juveniles are fully independent and may start forming pairs in the wild (Zann 1996). Accordingly, juveniles seem to be less motivated than fledglings to react to their parents’ vocalizations. But the persistence of the motivation to react preferentially towards parental calls in the absence of parental care is somewhat puzzling. Furthermore, this preference towards parental signals seems to undergo a subtle pattern of modification that may be directly linked to the transition to independence, a stage where acoustic cues such as distance calls may be essential to handle social relationships. Female zebra finches have been repeatedly shown to recognize and prefer the song of their father in the long term (Miller 1979; Clayton 1988; Riebel et al. 2002), and preferential response to the father’s distance calls in 2-month-old female juveniles may therefore be another aspect of this behaviour. Such kin recognition may be required for other behaviours, such as mate choice and inbreeding avoidance. Indeed, there is accumulating evidence that birds do not pair randomly, but may prefer to mate with nonrelatives and/or individuals carrying different genotypes (e.g. Blomqvist et al. 2002; Foerster et al. 2003; Freeman-Gallant et al. 2003; Mulard et al. 2009), with the presence of relatives in the neighbourhood potentially affecting dispersal behaviours (Daniels & Walters 2000). Such mate choice patterns generally imply that individuals are still able to recognize and avoid their kin at breeding age. There may be sex differences in the costs of inbreeding, a pattern which fits nicely with this sex difference which emerges at 2 months of age, when females are reaching sexual maturity. Transition to independence is generally linked to the development of foraging skills (e.g. Wheelwright & Templeton 2003; Polito & Trivelpiece 2008) and to the development of novel vocalizations (e.g. in the zebra finch: directed and undirected songs, distance calls, etc.; Zann 1996). Here we found that this transition was also accompanied by the development of sex-specific reactions to the calls of adults of the opposite sex. Young females still reacted preferentially to the calls of their father, whereas young males did not and all juveniles increased their reactivity to nonparent female calls. These differences may mark the appearance of sex-specific adult behaviours, with both sexes reacting more to females’ calls (Vicario et al. 2001) and females showing a preference for their father’s vocalizations. Overall, our results show that juvenile zebra finches were able to recognize their parents at fledging. Part of this call recognition was still present at pairing age and, like song recognition, may potentially persist in the long term. Transition to independence was accompanied by the appearance of sex-specific behaviours. The sexual and developmental status of the test bird is therefore an important factor explaining variation in response behaviours to

The two aims of these experiments were (1) to investigate recognition of parental distance calls by fledglings and almost sexually mature juveniles, and (2) to look at the development of response behaviours towards different stimuli between fledging and young adult stage. We showed that fledglings recognized both their father’s and mother’s calls, calling back preferentially to their parental calls than to the calls of other familiar adults. In the zebra finch, fledging occurs between 16 and 22 days of age, and parental care may still occur during the 20 days following fledging (Zann 1996). Since fledglings may form crèches of individuals of the same age (Zann 1996), recognition of their feeding parents may be important to direct parental care and to avoid both the costs and possible aggression of begging to nonparent adults. We found that fledglings reacted more to their father than to their mother, in contrast to adults which react more to female calls (Vicario et al. 2001; Gobes et al. 2009). Female distance calls show higher heritability and lower interindividual variance than male calls (Zann 1996; Forstmeier et al. 2009). It could thus be easier for fledglings to discriminate their father among other males. Alternatively, males may be less prone to care for their offspring, needing therefore to be more stimulated by young than females. Fledglings may thus have to call more to attract paternal attention and/or response. Indeed, it has been shown that females care more for their offspring than males in domestic but not in wild zebra finches (Zann 1996), losing more weight during chick rearing than males (Skagen 1988) and continuing to feed their chicks even in the absence of their mate, which does not occur in males (Royle et al. 2004, 2006). Recognition of parents by fledglings has been studied in numerous bird species, and seems to be a common feature in colonial species such as various swallows (Stoddard & Beecher 1983; Sieber 1985; Medvin & Beecher 1986; Beecher 1990; Leonard et al. 1997), jays (McArthur 1982) and seabirds (Beer 1969; Evans 1970; Charrier et al. 2001; Aubin & Jouventin 2002a; Mulard et al. 2008). Our study confirms this general view, but also clearly indicates that this recognition may continue in the long term, potentially having

Table 6 Statistical analysis of the effect of playback stimuli and chick stage (fledging or 2 months) on behavioural response (number of calls and latency to first call): random effects Random effects

Individual Brood identity Residual

Number of calls

Latency to first call

Variance

SD

Variance

SD

2.1 1.0 22.3

1.4 1.0 4.7

15.3 1.6 85.6

3.9 1.3 9.3

Linear mixed models were performed using the lmer() function of the lme4 package in R software.

Table 7 Statistical analysis of the effect of playback stimuli and chick stage (fledging or 2 months) on behavioural response (number of calls and latency to first call): fixed effects Fixed effects

Intercept Order SS Nature SC Stage Nature*Stage SS*Stage SC*Stage

Number of calls

Latency to first call

Estimate

SE

t

P

Estimate

SE

t

P

1.3 0.015 &0.52 0.74 &0.30 &2.2 3.6 2.7 0.93

0.72 0.098 0.47 0.47 0.78 0.64 0.66 0.66 0.67

1.8 0.15 &1.1 1.6 &0.40 &3.4 5.4 4.1 1.4

0.067 0.88 0.27 0.12 0.70 0.0007 <0.0001 <0.0001 0.16

18.0 0.30 3.2 &3.6 1.0 6.4 &4.8 &5.1 &2.0

1.5 0.19 0.92 0.92 1.7 1.3 1.3 1.3 1.3

12.2 1.6 3.5 &3.9 0.57 5.1 &3.7 &3.9 &1.5

<0.0001 0.12 0.0005 0.0001 0.57 <0.0001 0.0003 0.0001 0.13

Linear mixed models were performed using the lmer() function of the lme4 package in R software. P values were obtained using Markov chain Monte Carlo simulations (pvals.fnc() function). Significant P values are displayed in bold. Fixed-effects variables are abbreviated as in Table 3.

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