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 2   Mate recognition by female zebra finch: Analysis of individuality in

 3        male call and first investigations on female decoding process

 4

 5             Clémentine Vignala, Nicolas Mathevona,b*, Stéphane Mottinc

 6

 7

 8a Université Jean Monnet, laboratoire ‘Ecologie & Neuro-Ethologie Sensorielles’, EA3988, 23

 9rue Michelon, 42023 Saint-Etienne cedex 02, France

10

11b Université Paris-XI, The BioAcoustics Team, NAMC CNRS UMR 8620,Orsay, France

12

13c Université Jean Monnet, Laboratoire Hubert Curien, CNRS UMR 5516, Saint-Etienne, France

14

15*corresponding author

16E-mail address: mathevon@univ-st-etienne.fr




 1                                                                                              1
17Abstract

18

19        Zebra finches are monogamous birds living in large assemblies which represent a source

20of confusion for recognition between mates. Because the members of a pair use distance calls to

21remain in contact, call-based mate recognition is highly probable in this species. Whereas it had

22been previously demonstrated in males (Vignal et al., 2004), call-based mate recognition by

23females remained to be shown in females. By analysing the acoustic structure of male calls, we

24investigated the existence of an individual signature and identified the involved acoustic cues.

25We tested to see if females can identify their mates on the basis of their calls alone, and

26performed preliminary experiments using modified signals to investigate the acoustic basis of this

27recognition. Playback tests carried on 6 individuals showed that a female zebra finch is able to

28perform the call-based recognition of its mate. Our experiments suggested that the female uses

29both the energy spectrum and the frequency modulation of the male signal. More experiments are

30now needed to decipher precisely which acoustic cues are used by females for recognition.

31

32Keywords: Acoustic communication, individual recognition, mate, songbird, zebra finch




 2                                                                                                    2
331. Introduction

34

35      In flock-forming monogamous birds, mate recognition has to be performed at short as well

36as long ranges. Indeed, mate recognition may occur without site attachment when the flock is

37foraging or feeding. Since acoustic cues are efficient over short and long distances, individual

38vocal recognition seems to be a key component of pair-bond maintenance in birds (Beer, 1970;

39Clayton, 1990; Marzluff, 1988; Robertson, 1996). Zebra finches (Taeniopygia guttata castanotis)

40are gregarious songbirds of subarid regions of Australia, which form life-long pair bonds and

41breed in loose colonies (Butterfield, 1970; Zann, 1996). Among the number of different

42vocalizations produced by this species, distance calls are the most frequently emitted by both

43sexes. Male and female use distance calls to remain in contact especially when the birds are

44visually isolated from their mate during flock foraging (Zann, 1996). Distance calls are known to

45impart information on species, subspecies and geographical origins as well as sexual and

46individual identity (Zann, 1984; Okanoya and Dooling, 1991; Vicario et al., 2001). Contrary to

47females (Zann, 1996), males learn their call through a process of vocal imitation which explains

48that the calls of different males are acoustically distinct (Zann, 1984; Simpson and Vicario, 1990;

49Vicario et al., 2001). In spite of their unlearned origin, female distance calls have been shown to

50be clearly individualized and used by males for mate recognition (Vignal et al., 2004). On the

51contrary, no experiment has demonstrated that the learned distance calls of male zebra finches

52can support mate recognition by females, which is thought to rely on male song (Miller, 1979).

53There is a lack of playback experiments testing whether female zebra finches use call-based mate

54recognition and how the individual signature of male calls is used by females.

55      A songbird vocalization may support individual recognition if it shows a highly

56individualized acoustic structure allowing accurate discrimination from the remaining


 3                                                                                                      3
57conspecifics. In order to encode individual identity, an acoustic cue needs thus to present

58variation within individuals smaller than variation among individuals (Robisson et al., 1993;

59Mathevon, 1996; Charrier et al., 2002; Bloomfield et al. 2004 ; Charrier et al., 2004). In

60numerous colonial bird species, individual vocal signature is known to rely on the temporal

61pattern of frequency modulation and/or on the energy spectrum (Okanoya and Dooling, 1991;

62Jouventin et al., 1999; Lengagne et al., 2000, 2001; Charrier et al., 2001; Aubin and Jouventin,

632002; Aubin, 2004; Aubin et al., 2007). As the distance call of male zebra finches is a complex

64sound, typically a frequency modulated downsweep of a fundamental frequency and several

65associated harmonics (Zann, 1984; Simpson and Vicario, 1990), it may contain various acoustic

66cues capable of supporting individual identity.

67        The present study aimed first to investigate which acoustic parameters in the male

68distance call are likely to be involved in individual identity coding. Second, we tested to see

69whether females can identify their mates on the basis of their calls alone. Finally, we performed

70preliminary experiments using modified signals to investigate which acoustic cues are used in

71mate recognition.

72

732. Materials and methods

74

752.1. Subjects

76

77        Adult zebra finches Taeniopygia guttata castanotis (n = 6 pairs, i.e., 6 males and 6

78females) served as the subjects for this study and were naïve to all testing procedures. These birds

79were bred in an aviary of 60 birds (12L/12D photoperiod); food and water was provided ad

80libitum and temperature was maintained between 23 and 25°C. All birds were paired for several


 4                                                                                                    4
81months, in separate pair-cages allowing visual and acoustic contact with all the birds in the

 82aviary. Before the tests, each pair raised at least one brood (brood size = 2.33 ± 0.47 chicks). All

 83experiments occurred between 0900-1200 hrs. During testing periods, temperature, food and

 84water conditions were the same as in the aviary. The experimental protocols were approved by

 85the Jean Monnet University’s animal care committee.

 86

 872.2. Recording of male calls and analysis of acoustic parameters

 88

 89The six male zebra finches were recorded for analysis of male distance calls. Each male was

 90isolated from its mate and seven to ten distance calls were recorded with a Sennheiser MD42

 91microphone, placed 0.3m above the cage, connected to a Marantz PMD690/W1B recorder with

 9222,050 Hz sampling rate. We analysed a total of 55 male distance calls using Syntana software

 93(Aubin, 1994) and Praat version 4.0.19 (www.praat.org). We defined eighteen spectral, temporal

 94and amplitude acoustic cues to describe the calls’ acoustic structure.

 95        The zebra finch distance call is a complex sound with a fundamental frequency associated

 96with several harmonics (Figure 1a). This sound is frequency and amplitude modulated. The male

 97distance call has an elevated fundamental frequency (600-1000 Hz) compared to the female one

 98(400-500 Hz). It is typically a frequency modulated downsweep of around 100 ms (Zann 1984;

 99Simpson and Vicario 1990; Vicario et al. 2001). In our population of zebra finches, the typical

100male distance call can be divided into two segments of different durations (Figure 1a): a first

101segment composed by an initial rapid ascending frequency modulation of low amplitude followed

102by a short stable part (the tonal component defined by Zann 1984), and a second segment defined

103by a long and loud descending frequency modulation (the noise component or downsweep

104component defined by Zann 1984).


  5                                                                                                       5
105        To describe the frequency modulation of the call, we first isolated the fundamental

106frequency using the cepstrum method (Aubin, 1994). Three temporal parameters were measured

107from the fundamental frequency (Figure 1b): the duration of the ascending frequency modulation

108of the tonal component (dasc, s), the duration of the stable part of the tonal component (dstab, s),

109and the duration of the descending frequency modulation of the downsweep component (ddesc,

110s). Four spectral parameters were also measured from the fundamental frequency (Figure 1b): the

111start frequency (Fstart, Hz), the frequency of the beginning of the stable part (Fstab1, Hz), the

112frequency of the end of the stable part (Fstab2, Hz), and the end frequency of the call (Fend, Hz).

113These parameters were used to calculate the two following parameters: Fmasc, the slope of the

114ascending frequency modulation (Hz s-1) [calculated as (Fstab1-Fstart)/dasc], and Fmdesc, the

115slope of the descending frequency modulation (Hz s-1) [calculated as (Fend-Fstab2)/ddesc].

116        To describe the amplitude change over time, we measured three parameters from the

117envelope of the signal (Figure 1c): the mean intensity of the entire call represented by the root-

118mean-square signal level (RMSaver, dB), the highest amplitude in the call (RMSmax, Pa) and the

119duration between the beginning of the call and the time at which the highest amplitude in the call

120occurs (Tmax, s). We then calculated the parameter RMSmax/ RMSaver.

121        To describe the energy spectrum of the call, measures were performed on the Fast Fourier

122Transform (FFT) of the signal. The percentage of energy in each interval of 1000 Hz was

123assessed. We then quantified six energy intervals corresponding to the percentage of energy of

124the call between 0 and 1000 Hz (Band 1), 1000-2000 Hz (Band 2), 2000-3000 Hz (Band 3),

1253000-4000 Hz (Band 4), 4000-5000 Hz (Band 5) and 5000-6000 Hz (Band 6).

126        Two parameters were measured from the average power spectrum calculated from the

127total length of the call with the LPC method (Applying linear predictive coding) (Figure 1d): the




  6                                                                                                     6
128frequency of the first peak amplitude (Fmax, Hz) and the intensity of this peak (Imax, dB) which

129is normalised by calculating the ratio Imax/ RMSaver.

130

1312.3. Statistical analysis of acoustic parameters

132

133These measured parameters allowed statistical analysis of the cues potentially supporting

134individual identity coding. We first performed a non-parametric analysis of variance (Kruskall-

135Wallis ANOVA, P = 0.05). To describe the intra-individual and inter-individual variations of

136each parameter we used the coefficient of variation (CV) (Sokal and Rolhf, 1995). For each

137parameter we calculated CVi (within individual CV) and CVb (between individual CV) according

138to the formula for small sample size:

139 CV = {100(SD/Xmean)[1+(1/4*n)]}

140where SD is standard deviation, Xmean is the mean of the sample and n is the sample size

141(Robisson et al. 1993). To assess the Potential for Individual Coding (PIC, Robisson et al., 1993)

142for each parameter, we calculated the ratio CVb/meanCVi (mean CVi being the mean value of the

143CVi of all individuals). For a given parameter, a PIC value greater than 1 suggests that this

144parameter may be used for individual recognition since its intra-individual variability is smaller

145than its inter-individual variability.

146        Besides this univariate analysis, we used a multivariate approach to test if calls could be

147reliably classified according to the identity of their emitter. This multivariate analysis was done

148on the variables that were identified as potentially relevant by the ANOVA (i.e., with P values

149<0.05). We transformed these variables into a set of non-correlated components using a principal

150component analysis (Beecher, 1989). We then a performed a discriminant analysis on the new

151data set.


  7                                                                                                      7
152All statistical tests were performed using Statistica software version 6.1.

153

1542.4. Playback procedure

155

156        For playback tests, each tested female (n = 6) was moved from the aviary and placed in an

157experimental cage (240 x 50 x 50 cm, equipped with roosts) one night prior to the start of

158stimulus presentation. The experimental cage was in a soundproof chamber with a 12L/12D

159photoperiod. Another cage was placed near the experimental cage in the chamber. According to

160the demonstrated effect of social context on the response of zebra finches to playback tests

161(Vignal et al., 2004), this companion cage contained one male-female pair and represented a

162simulated social context for the tested bird. As this audience was composed of different

163individuals during each trial, we can assume that the response of the tested birds were

164independent. All experiments occurred between 8 am and 10 am. The playback equipment

165consisted of a Marantz PMD690/W1B recorder and an amplifier (Yamaha AX-396) connected to

166two high fidelity speakers (Triangle Comete 202) placed at either end of the cage. During each

167test, only one randomly chosen speaker emitted the playback stimuli (sound level: 70 dB(A) SPL

168at 1 meter; each experimental signal was rescaled to match the root mean square amplitude of the

169control signal in order to get the same output level). The tested bird was presented with eight

170series of stimuli: one series of synthetic copies of natural distance calls of its mate (positive

171control), one series of synthetic copies of natural distance calls of a familiar male (negative

172control), and six experimental series of modified mate distance calls (in each series: calls played

173at natural rates, i.e., 2 calls.s-1; series broadcast at random; series duration: 10 seconds; interval

174between series: 30 seconds).




  8                                                                                                         8
175        As the birds (recorded males, audience birds, and tested females) had been bred in the

176same aviary, all acoustic stimuli can be considered as perceptually equivalent for all of the birds.

177

1782.5. Playback experiments

179

1802.5.1. Experimental signals

181

182        A synthetic copy of one distance call (selected at random) of each recorded bird (n=6

183males, same individuals as those used for analysis) was created using the graphic synthesizer

184module of Avisoft-SAS Lab-Pro software (version 4.16, 2002). The copies were built to match as

185accurately as possible the acoustic characteristics of the original signals. As most of the energy in

186male distance calls is encompassed by seven harmonics in our population of zebra finches, all

187copies were synthesized with seven harmonics. These synthetic control copies were used to

188address the following questions.

189

1902.5.2. Do female zebra finches respond selectively to their mate voice?

191

192        To test the ability of female zebra finches to discriminate their mate among others, we

193played back to the females a series of 20 synthetic copies of male calls from their own mate and a

194series of 20 synthetic copies of calls from a familiar male. To rule out effects of particular

195individuals and limit the risk of pseudoreplication during playback experiments (McGregor et al.,

1961992), each female was tested with calls from different familiar males.




  9                                                                                                    9
197

1982.5.3. What are the acoustic cues used by the female for mate recognition?

199

200        In order to decipher how females identify a caller using the acoustic structure of its call,

201we used modified mate calls whose original characteristics were mixed with calls features of a

202familiar male.

203

204Modifications of the temporal structure: we replaced temporal elements of the mate call with

205those of a familiar male. The first experimental signal was built using the tonal component of the

206mate call associated with the downsweep component of the call of a familiar male (signals TM,

207Figure 2a) ; the second experimental signal was built using the tonal component of a familiar

208male call associated with the downsweep component of the mate call (signals TF, Figure 2a).

209Because the most individualized part of the male call is the downsweep component (see Results),

210we tested whether this part alone (signals DS, Figure 2a) is sufficient to evoke selective response

211from the female. All the following signal modifications concern this final downsweep component

212alone. For each modification, we chose to replace the initial mate call parameter by the same

213parameter measured in the call of a familiar male.

214

215Modification of the fundamental frequency: the fundamental frequency of the mate call was

216shifted to reach the mean values of fundamental frequency of the familiar male call (signals FF,

217Figure 2b). The natural amplitude envelope, the energy spectrum and temporal structures of the

218mate call remained unchanged.

219




 10                                                                                                       10
220Modification of the frequency modulation: the slope of frequency modulation of the fundamental

221frequency of the mate call was modified to reach the slope of frequency modulation of the

222fundamental frequency of a familiar male call (signals FM), Figure 2b). The natural amplitude

223envelope, the energy spectrum and the natural mean fundamental frequency remained unchanged.

224

225Modification of the energy spectrum: the natural energy spectrum of the final downsweep

226component of the mate call was replaced with the energy spectrum of a familiar male call (signals

227ES, Figure 2b). The natural amplitude and frequency structures remained unchanged.

228

2292.6. Criteria of Response

230

231        During the playback test, the vocal and locomotor activity of the tested bird was

232monitored with a video recorder (SONY DCR-TRV24E). We measured the latency of the vocal

233response (LR in seconds) and the number of distance calls emitted during the broadcasting of the

234stimuli (NC). Prior to the beginning of playback broadcasting, we made sure that the bird

235spontaneous activity was low (no vocalizations emitted during the minute that preceeded the

236experiment).

237

2382.7. Statistical Analysis of playback experiments

239

240        When a female showed a shorter latency (LR) and/or a greater number of calls (NC) in

241response to mate calls than to familiar male calls, its response was considered as a mate

242recognition behaviour. To assess the effectiveness of mate call recognition by female zebra




 11                                                                                                11
243finches, the number of females showing a mate recognition behaviour was compared to the

244number of females showing no mate-directed behaviour using binomial test.

245

246        To assess the behavioural response to experimental (modified) signals and mate calls, we

247defined two ratios of reference: 1) the reference latency ratio = (LR in response to familiar

248calls) / (LR in response to mate calls); 2) the reference calling ratio = (NC in response to mate

249calls + 1) / (NC in response to familiar calls + 1). A mate recognition behaviour was expressed as

250follows: reference latency ratio + reference calling ratio e 2. For each tested modification and for

251each bird, we defined the two following ratios: 1) the latency ratio = (LR in response to modified

252calls) / (LR in response to mate calls); 2) the calling ratio = (NC in response to modified calls +

2531) / (NC in response to familiar calls + 1). These ratios were compared to the reference ratios. If

254latency ratio > reference latency ratio, the stimulus received 0 point, if latency ratio < reference

255latency ratio, the stimulus received 2 points, and if latency ratio < reference latency ratio but is

256bigger than one, the stimulus received 1 point. In case of no response to a stimulus, no point was

257assigned to this stimulus. If calling ratio > reference calling ratio, the stimulus received 2 point, if

258calling ratio < reference calling ratio, the stimulus received 0 point, and if calling ratio <

259reference calling ratio but is bigger than one, the stimulus received 1 point. In case of no

260response to a stimulus, no point was obtained by this stimulus. A stimulus was considered to

261induce a mate recognition behaviour if its total score was e 2. To compare the number of

262recognition responses obtained by modified calls with the number of recognition responses

263obtained by control mate calls, we used Wilcoxon paired-samples tests with a Bonferroni

264correction for multiple tests.

265




 12                                                                                                       12
2663. Results

267

2683.1. Description of male calls and potential for individual identity coding

269

270        The fundamental frequency of the distance call of the male zebra finch has a mean start

271frequency of 730 Hz (Table 1), its short stable part (mean duration .018 s) presents a mean

272frequency between 827 and 1031 Hz, and its mean end frequency is of 509 Hz. Thus, the call is

273frequency modulated, with a mean ascending frequency modulation of the initial segment of

2743800 Hz.s-1 and a descending final segment with a mean frequency modulation of 5607 Hz.s-1.

275Most of the call energy is concentrated between 2000 and 4000 Hz (band 3 and 4) and the first

276peak of amplitude has a mean frequency of 2809 Hz. The call is amplitude modulated: the ratio

277RMSmax / RMS aver is different from 1. The highest peak of amplitude occurs during the final

278downsweep part.

279        As summarised in Table 1, all the measured parameters except dstab and Fmasc are

280significantly modified by the identity of the caller (Kruskal-Wallis ANOVA, p < .05). For all

281these parameters, the coefficients of variation within individuals are smaller than those among

282individuals: all the parameters except dstab and Fmasc are potential cues for individual identity

283coding. The PIC values of two frequency parameters are greater than 2: the frequency of the end

284of the stable part (Fstab2) and the slope of the descending frequency modulation (Fmdesc) are

285thus highly individualized. Three spectral parameters (bands 4, 5 and 6) present a PIC greater

286than 2: the energy spectrum of the call is thus well individualized.

287        The results of the multivariate approach also reveal an individual signature in the distance

288call of male zebra finches. Using the principal components calculated with the acoustic




 13                                                                                                    13
289parameters showing a significant between-individuals variation, we performed a discriminant

290analysis that separate 100% of the calls of the six males.

291

2923.2. Playback experiments

293

2943.2.1. Female zebra finches respond selectively to mate voice

295

296        Females responded with shorter latency (individuals f1, f2, f3, f5 and f6, Table 2) and/or

297with more calls (individuals f1, f3, f4, f5 and f6, Table 2) to mate calls than to familiar male

298calls, thus showing a mate recognition behaviour (mean latency to mate calls = 1.56±2.4 s, mean

299latency to familiar calls = 5.69±6.08 s ; mean number of calls in response to mate calls = 3.7±2,

300mean number of calls in response to familiar calls = 2.2±2 ; two-tailed binomial test P=0.03).

301The responses of all of the six tested females verified that reference latency ratio + reference

302calling ratio e 2.

303




 14                                                                                                   14
3043.2.2. Female recognition seems to be sensitive to frequency features alterations of mate call

305

306        Due to the small number of tested individuals, the results show only tendencies and are

307not supported by statistical validity (after Bonferroni corrections). Nevertheless, it appears that

308some of the modifications are likely to impair mate vocal recognition more deeply than others

309(Table 2).

310        The most reliable signals are those presenting temporal alterations. Four females among

311the six tested individuals showed a mate recognition behaviour in response to composite signals

312built using the association of the tonal component of the mate call and the final downsweep

313component of the call of a familiar male (signal TM) and three females recognized composite

314signals built using the association of the tonal component of a familiar male call and the final

315downsweep component of the mate call (signal TF). The final downsweep component alone

316(signal DS) elicited recognition response by four females among the six tested individuals.

317        Conversely, shifts of the fundamental frequency of the final downsweep component of the

318mate call (signal FF) elicited recognition response by only two females among the six tested

319individuals. Likewise, mate vocal recognition seems especially impaired when the frequency

320modulation or the energy spectrum of the mate call was replaced respectively by the frequency

321modulation or the energy spectrum of a familiar male call (signal FM). Indeed, only two females

322among the six tested individuals showed recognition responses in both situations.

323

3244. Discussion

325

3264.1. Acoustic features encoding individual signature in male distance calls

327


 15                                                                                                      15
328        The analysis of the distance calls of male zebra finches highlights that some acoustic

329parameters are likely to be used as cues for individual identity coding. Particularly, frequency

330parameters of the fundamental frequency of the call - like the frequency of the end of the stable

331part (Fstab2) and the slope of the descending frequency modulation (Fmdesc) - as well as spectral

332parameters - like the band energy between 3000 and 6000 Hz - are highly individualized.

333Consequently, information about individual identity is likely to be encoded in both spectral

334domain and temporal pattern: the energy spectrum of the call as well as the temporal pattern of

335frequency modulation of the final downsweep part are good candidates for individual identity

336coding. Frequency modulation is known to support acoustic coding of information in several bird

337species (Jouventin et al., 1999; Lengagne et al., 2000; Mathevon and Aubin, 2001; Charrier et al.,

3382001) but also in mammals (Charrier et al., 2002).

339        According to our analysis, some parameters are unlikely to encode individual identity.

340Temporal parameters like the duration of the stable part (dstab) or the slope of the ascending part

341of the call (Fmasc) are variable features both within individuals and among individuals. Such

342acoustic cues can not encode any information about the identity of the caller.

343        Consequently, we hypothesize that the acoustic parameters used by females to identify

344their mate may be characteristic of the well individualized final downsweep part of the call like

345(i) its frequency modulation, (ii) the absolute values of its fundamental frequency and (iii) its

346energy spectrum.

347

3484.2. Acoustic parameters used by female zebra finches for mate call recognition

349

350        Since only 6 females were tested and given the mixed results we obtained, it is difficult to

351sketch a precise picture of how females proceed to identify a caller. However, it remains possible


 16                                                                                                    16
352to draw a general tendency. First, mate vocal recognition seems to remain possible even if a part

353of the call is absent or modified. Second, whereas mate recognition can be performed using the

354downsweep part alone, modifications of its frequency modulation, its energy spectrum, or the

355absolute values of its fundamental frequency are likely to impair the recognition process. Given

356these results and the data from call analysis, females could use both the energy spectrum and the

357slope of frequency modulation of the downsweep part to identify the call of their mate. The vocal

358signature is certainly multi-parametric, presenting a redundancy between tonal and downsweep

359parts that allows females to compensate the absence of segments by using the remaining

360information. Given the high temporal and frequency discrimination abilities of zebra finches

361(e.g., Weisman et al. 1998, Lee et al. 2006, Lohr et al. 2006, Friedrich et al. 2007), this vocal

362recognition system is likely to be efficient in spite of the noisy environment of the colony.

363

3644.3. A vocal signature participating in pair-bond maintenance

365

366        As proposed by some authors, the maintenance of long-lasting pair bonds could avoid the

367necessity for active, elaborate display before breeding and thus could allow reducing activity and

368energy expenditure in an unpredictable environment (Davies, 1982). This could provide an

369evolutionary explanation for monogamy in species of arid areas like the zebra finch. Monogamy

370could thus provide a ready-to-use reproductive system, which could rapidly start breeding after

371uncertain rainfall periods (Cynx, 2001). In such opportunistic species, there is thus a need for a

372bird to efficiently recognize its mate during and outside the breeding season. Particularly,

373nomadic species like the zebra finch need to perform mate recognition without site fidelity. Some

374previous studies report that whereas tactile contact between mates is necessary in the process of

375pair-formation, established pair-bonds can be maintained by auditory contact alone between


 17                                                                                                     17
376mates (Silcox and Evans, 1982). Our results show that female zebra finches perform mate

377recognition using male calls. Nevertheless, it does not exclude that other sensory channels can be

378used for mate recognition, e.g., visual cues have been demonstrated to play a role in zebra finches

379pair bond maintenance (Butterfield, 1970).

380

381

382Acknowledgements

383

384We warmly thank Chris Sturdy for his welcome to contribute this modest paper in honour of Ron

385Weisman. This work was supported by the French National Research Agency (ANR, project

386‘BIRDS’VOICES’) and by the Program ‘Emergence’ of the Région Rhône-Alpes. NM is funded

387by the Institut universitaire de France (IUF). We are grateful to Colette Bouchut for technical

388assistance and Corinne Eyzac for taking care of the birds. Many thanks to Noémie Constant and

389Sébastien Tisseur for their help during the calls recording and analysis.




 18                                                                                                  18
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469Press, Oxford.




 22                                                                                                   22
470                                          Figures captions

471

472        Fig. 1. Acoustic structure of the distance call of a male zebra finch. (a) Spectrogram and

473oscillogram of the distance call. The distance call is composed of a fundamental frequency and

474several harmonics. It can be divided into a first segment (the Tonal component) composed by an

475initial rapid ascending frequency modulation of low amplitude followed by a short stable part,

476and a second segment defined by a long and loud descending frequency modulation (the

477Downsweep component). (b) Fundamental frequency of the call (obtained with the cepstrum

478method) used to describe the frequency modulation. We measured the duration of the ascending

479frequency modulation of the tonal component (dasc, s), the duration of the stable part of the tonal

480component (dstab, s), the duration of the descending frequency modulation of the downsweep

481component (ddesc, s), as well as the start frequency (Fstart, Hz), the frequency at the beginning

482of the stable part (Fstab1, Hz), the frequency at the end of the stable part (Fstab2, Hz), and the

483end frequency of the call (Fend, Hz). (c) Amplitude envelope of the call. The parameters

484measured were the mean intensity of the entire call (RMSaver, dB), the loudest intensity in the

485call (RMSmax, Pa) and the duration between the beginning of the call and the time at which the

486highest amplitude in the call occurs (Tmax, s). (d) Average power spectrum calculated from the

487total length of the call with the LPC method (linear predictive coding). The frequency of the first

488peak amplitude (Fmax, Hz) and the intensity of this peak (Imax, dB) were measured.

489

490Fig. 2. Spectrograms of a male distance call and experimental modified calls. (a) Control male

491call (mate call) and calls presenting modifications of their temporal structure. TM : the tonal

492component of the mate call is associated with the final downsweep component of the call of a

493familiar male. TF : the tonal component of a familiar male call is associated with the final


 23                                                                                                     23
494downsweep component of the call of the mate. DS : the final downsweep component of the mate

495call is tested alone. (b) The final downsweep component (DS) of the mate call and its

496modifications in the frequency and the time domains. FF: shift of the fundamental frequency.

497FM: Modification of the frequency modulation. ES: Modification of the energy spectrum.




 24                                                                                               24
498

499

500

501Figure 1




 25           25
502




503

504

505Figure 2




 26           26
506

                                   Standard                                       PIC Kruskal-Wallis
Variable                 Mean                   Mean CVi        CVb
                                  Deviation                            CVb / mean CVi        P value
dstab (s)                 0.018       0.006          36,5      33,61             0,92         p > .05
Tmax (s)                0.05465    0.02028          26,77      37,28             1,39              *
Fstart (Hz)                730         25.1          2,77       3,47             1,25              *
Fstab1 (Hz)                827          17           1,67       2,07             1,24              *
Fstab2 (Hz)               1031        313.3          3,44      30,53             8,87              *
Fend (Hz)                  509          54           7,19      10,66             1,48              *
Fmasc (Hz.s-1)            3800        845.5         22,46      22,44             1,00         p > .05
Fmdesc (Hz.s-1)           5607        1883          12,46      33,74             2,71              *
RMSmax/ RMSaver          0.0056     0.0024          28,47      43,05             1,51              *
Imax / RMSaver            0.741     0.0453           3,59       6,14             1,71              *
Fmax (Hz)                 2809        309.5          7,77      11,07             1,42              *
Band1 (%)                  0.29        0.29         61,51     100,45             1,63              *
Band2 (%)                   2.7         2.4         48,67      89,29             1,83              *
Band3 (%)                   37          21          41,71      57,01             1,37              *
Band4 (%)                   52          59             46     113,98             2,48              *
Band5 (%)                   17          38          58,92     224,55             3,81              *
Band6 (%)                   5.5         14          70,08     255,70             3,65              *
 507

508

509Table 1

510Analysis of the individuality of the acoustic parameters of the male distance call. To describe the

511intra-individual and inter-individual variations of each parameter we used the coefficient of

512variation (CV) (Sokal & Rolhf, 1995). For each parameter we calculated CVi (within individual

513CV) and CVb (between individual CV). * corresponds to p < .05. Bold PIC values correspond to

514PIC > 2.




  27                                                                                                    27
515


                                                                   Total
                   LR      LR reference NC           NC reference         Total Total Total Total Total Total
Tested                                                             score
                  mate familiar latency mate     familiar calling         score score score score score score
females                                                               of
                  calls   calls    ratio calls      calls    ratio       of TM of TF of DS of FF of MF of ES
                                                                   mate

f1                0,356   1,579     4,43    5          2        2     2     3      1      2      0      0      0
f2                 0,33   1,579     4,78    2          6     0,43     2     0      4      0      0      2      0
f3                1,705   16,59     9,73    1          0        2     2     0      3      3      0      1      1
f4                0,449   0,376     0,84    6          2     2,33     2     4      1      2      0      0      3
f5                0,172   6,446    37,48    5          1        3     2     2      2      2      2      2      2
f6                6,326   7,562     1,19    3          2     1,33     2     3      0      0      4      0      0
number of
females
performing mate                                                       6     4      3      4      2      2      2
recognition
P value                                                                   0.89   0.79   0.29   0.22   0.07   0.11
(Wilcoxon test)
516

517

518Table 2

519Responses of females to mate calls, familiar calls and modified mate calls. LR: latency of the

520vocal response (in seconds), NC: number of distance calls emitted during the broadcasting of the

521stimulus.




 28                                                                                                                 28

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Vignal-mathevon-mottin 2008 behavioural processes

  • 1. 1 2 Mate recognition by female zebra finch: Analysis of individuality in 3 male call and first investigations on female decoding process 4 5 Clémentine Vignala, Nicolas Mathevona,b*, Stéphane Mottinc 6 7 8a Université Jean Monnet, laboratoire ‘Ecologie & Neuro-Ethologie Sensorielles’, EA3988, 23 9rue Michelon, 42023 Saint-Etienne cedex 02, France 10 11b Université Paris-XI, The BioAcoustics Team, NAMC CNRS UMR 8620,Orsay, France 12 13c Université Jean Monnet, Laboratoire Hubert Curien, CNRS UMR 5516, Saint-Etienne, France 14 15*corresponding author 16E-mail address: mathevon@univ-st-etienne.fr 1 1
  • 2. 17Abstract 18 19 Zebra finches are monogamous birds living in large assemblies which represent a source 20of confusion for recognition between mates. Because the members of a pair use distance calls to 21remain in contact, call-based mate recognition is highly probable in this species. Whereas it had 22been previously demonstrated in males (Vignal et al., 2004), call-based mate recognition by 23females remained to be shown in females. By analysing the acoustic structure of male calls, we 24investigated the existence of an individual signature and identified the involved acoustic cues. 25We tested to see if females can identify their mates on the basis of their calls alone, and 26performed preliminary experiments using modified signals to investigate the acoustic basis of this 27recognition. Playback tests carried on 6 individuals showed that a female zebra finch is able to 28perform the call-based recognition of its mate. Our experiments suggested that the female uses 29both the energy spectrum and the frequency modulation of the male signal. More experiments are 30now needed to decipher precisely which acoustic cues are used by females for recognition. 31 32Keywords: Acoustic communication, individual recognition, mate, songbird, zebra finch 2 2
  • 3. 331. Introduction 34 35 In flock-forming monogamous birds, mate recognition has to be performed at short as well 36as long ranges. Indeed, mate recognition may occur without site attachment when the flock is 37foraging or feeding. Since acoustic cues are efficient over short and long distances, individual 38vocal recognition seems to be a key component of pair-bond maintenance in birds (Beer, 1970; 39Clayton, 1990; Marzluff, 1988; Robertson, 1996). Zebra finches (Taeniopygia guttata castanotis) 40are gregarious songbirds of subarid regions of Australia, which form life-long pair bonds and 41breed in loose colonies (Butterfield, 1970; Zann, 1996). Among the number of different 42vocalizations produced by this species, distance calls are the most frequently emitted by both 43sexes. Male and female use distance calls to remain in contact especially when the birds are 44visually isolated from their mate during flock foraging (Zann, 1996). Distance calls are known to 45impart information on species, subspecies and geographical origins as well as sexual and 46individual identity (Zann, 1984; Okanoya and Dooling, 1991; Vicario et al., 2001). Contrary to 47females (Zann, 1996), males learn their call through a process of vocal imitation which explains 48that the calls of different males are acoustically distinct (Zann, 1984; Simpson and Vicario, 1990; 49Vicario et al., 2001). In spite of their unlearned origin, female distance calls have been shown to 50be clearly individualized and used by males for mate recognition (Vignal et al., 2004). On the 51contrary, no experiment has demonstrated that the learned distance calls of male zebra finches 52can support mate recognition by females, which is thought to rely on male song (Miller, 1979). 53There is a lack of playback experiments testing whether female zebra finches use call-based mate 54recognition and how the individual signature of male calls is used by females. 55 A songbird vocalization may support individual recognition if it shows a highly 56individualized acoustic structure allowing accurate discrimination from the remaining 3 3
  • 4. 57conspecifics. In order to encode individual identity, an acoustic cue needs thus to present 58variation within individuals smaller than variation among individuals (Robisson et al., 1993; 59Mathevon, 1996; Charrier et al., 2002; Bloomfield et al. 2004 ; Charrier et al., 2004). In 60numerous colonial bird species, individual vocal signature is known to rely on the temporal 61pattern of frequency modulation and/or on the energy spectrum (Okanoya and Dooling, 1991; 62Jouventin et al., 1999; Lengagne et al., 2000, 2001; Charrier et al., 2001; Aubin and Jouventin, 632002; Aubin, 2004; Aubin et al., 2007). As the distance call of male zebra finches is a complex 64sound, typically a frequency modulated downsweep of a fundamental frequency and several 65associated harmonics (Zann, 1984; Simpson and Vicario, 1990), it may contain various acoustic 66cues capable of supporting individual identity. 67 The present study aimed first to investigate which acoustic parameters in the male 68distance call are likely to be involved in individual identity coding. Second, we tested to see 69whether females can identify their mates on the basis of their calls alone. Finally, we performed 70preliminary experiments using modified signals to investigate which acoustic cues are used in 71mate recognition. 72 732. Materials and methods 74 752.1. Subjects 76 77 Adult zebra finches Taeniopygia guttata castanotis (n = 6 pairs, i.e., 6 males and 6 78females) served as the subjects for this study and were naïve to all testing procedures. These birds 79were bred in an aviary of 60 birds (12L/12D photoperiod); food and water was provided ad 80libitum and temperature was maintained between 23 and 25°C. All birds were paired for several 4 4
  • 5. 81months, in separate pair-cages allowing visual and acoustic contact with all the birds in the 82aviary. Before the tests, each pair raised at least one brood (brood size = 2.33 ± 0.47 chicks). All 83experiments occurred between 0900-1200 hrs. During testing periods, temperature, food and 84water conditions were the same as in the aviary. The experimental protocols were approved by 85the Jean Monnet University’s animal care committee. 86 872.2. Recording of male calls and analysis of acoustic parameters 88 89The six male zebra finches were recorded for analysis of male distance calls. Each male was 90isolated from its mate and seven to ten distance calls were recorded with a Sennheiser MD42 91microphone, placed 0.3m above the cage, connected to a Marantz PMD690/W1B recorder with 9222,050 Hz sampling rate. We analysed a total of 55 male distance calls using Syntana software 93(Aubin, 1994) and Praat version 4.0.19 (www.praat.org). We defined eighteen spectral, temporal 94and amplitude acoustic cues to describe the calls’ acoustic structure. 95 The zebra finch distance call is a complex sound with a fundamental frequency associated 96with several harmonics (Figure 1a). This sound is frequency and amplitude modulated. The male 97distance call has an elevated fundamental frequency (600-1000 Hz) compared to the female one 98(400-500 Hz). It is typically a frequency modulated downsweep of around 100 ms (Zann 1984; 99Simpson and Vicario 1990; Vicario et al. 2001). In our population of zebra finches, the typical 100male distance call can be divided into two segments of different durations (Figure 1a): a first 101segment composed by an initial rapid ascending frequency modulation of low amplitude followed 102by a short stable part (the tonal component defined by Zann 1984), and a second segment defined 103by a long and loud descending frequency modulation (the noise component or downsweep 104component defined by Zann 1984). 5 5
  • 6. 105 To describe the frequency modulation of the call, we first isolated the fundamental 106frequency using the cepstrum method (Aubin, 1994). Three temporal parameters were measured 107from the fundamental frequency (Figure 1b): the duration of the ascending frequency modulation 108of the tonal component (dasc, s), the duration of the stable part of the tonal component (dstab, s), 109and the duration of the descending frequency modulation of the downsweep component (ddesc, 110s). Four spectral parameters were also measured from the fundamental frequency (Figure 1b): the 111start frequency (Fstart, Hz), the frequency of the beginning of the stable part (Fstab1, Hz), the 112frequency of the end of the stable part (Fstab2, Hz), and the end frequency of the call (Fend, Hz). 113These parameters were used to calculate the two following parameters: Fmasc, the slope of the 114ascending frequency modulation (Hz s-1) [calculated as (Fstab1-Fstart)/dasc], and Fmdesc, the 115slope of the descending frequency modulation (Hz s-1) [calculated as (Fend-Fstab2)/ddesc]. 116 To describe the amplitude change over time, we measured three parameters from the 117envelope of the signal (Figure 1c): the mean intensity of the entire call represented by the root- 118mean-square signal level (RMSaver, dB), the highest amplitude in the call (RMSmax, Pa) and the 119duration between the beginning of the call and the time at which the highest amplitude in the call 120occurs (Tmax, s). We then calculated the parameter RMSmax/ RMSaver. 121 To describe the energy spectrum of the call, measures were performed on the Fast Fourier 122Transform (FFT) of the signal. The percentage of energy in each interval of 1000 Hz was 123assessed. We then quantified six energy intervals corresponding to the percentage of energy of 124the call between 0 and 1000 Hz (Band 1), 1000-2000 Hz (Band 2), 2000-3000 Hz (Band 3), 1253000-4000 Hz (Band 4), 4000-5000 Hz (Band 5) and 5000-6000 Hz (Band 6). 126 Two parameters were measured from the average power spectrum calculated from the 127total length of the call with the LPC method (Applying linear predictive coding) (Figure 1d): the 6 6
  • 7. 128frequency of the first peak amplitude (Fmax, Hz) and the intensity of this peak (Imax, dB) which 129is normalised by calculating the ratio Imax/ RMSaver. 130 1312.3. Statistical analysis of acoustic parameters 132 133These measured parameters allowed statistical analysis of the cues potentially supporting 134individual identity coding. We first performed a non-parametric analysis of variance (Kruskall- 135Wallis ANOVA, P = 0.05). To describe the intra-individual and inter-individual variations of 136each parameter we used the coefficient of variation (CV) (Sokal and Rolhf, 1995). For each 137parameter we calculated CVi (within individual CV) and CVb (between individual CV) according 138to the formula for small sample size: 139 CV = {100(SD/Xmean)[1+(1/4*n)]} 140where SD is standard deviation, Xmean is the mean of the sample and n is the sample size 141(Robisson et al. 1993). To assess the Potential for Individual Coding (PIC, Robisson et al., 1993) 142for each parameter, we calculated the ratio CVb/meanCVi (mean CVi being the mean value of the 143CVi of all individuals). For a given parameter, a PIC value greater than 1 suggests that this 144parameter may be used for individual recognition since its intra-individual variability is smaller 145than its inter-individual variability. 146 Besides this univariate analysis, we used a multivariate approach to test if calls could be 147reliably classified according to the identity of their emitter. This multivariate analysis was done 148on the variables that were identified as potentially relevant by the ANOVA (i.e., with P values 149<0.05). We transformed these variables into a set of non-correlated components using a principal 150component analysis (Beecher, 1989). We then a performed a discriminant analysis on the new 151data set. 7 7
  • 8. 152All statistical tests were performed using Statistica software version 6.1. 153 1542.4. Playback procedure 155 156 For playback tests, each tested female (n = 6) was moved from the aviary and placed in an 157experimental cage (240 x 50 x 50 cm, equipped with roosts) one night prior to the start of 158stimulus presentation. The experimental cage was in a soundproof chamber with a 12L/12D 159photoperiod. Another cage was placed near the experimental cage in the chamber. According to 160the demonstrated effect of social context on the response of zebra finches to playback tests 161(Vignal et al., 2004), this companion cage contained one male-female pair and represented a 162simulated social context for the tested bird. As this audience was composed of different 163individuals during each trial, we can assume that the response of the tested birds were 164independent. All experiments occurred between 8 am and 10 am. The playback equipment 165consisted of a Marantz PMD690/W1B recorder and an amplifier (Yamaha AX-396) connected to 166two high fidelity speakers (Triangle Comete 202) placed at either end of the cage. During each 167test, only one randomly chosen speaker emitted the playback stimuli (sound level: 70 dB(A) SPL 168at 1 meter; each experimental signal was rescaled to match the root mean square amplitude of the 169control signal in order to get the same output level). The tested bird was presented with eight 170series of stimuli: one series of synthetic copies of natural distance calls of its mate (positive 171control), one series of synthetic copies of natural distance calls of a familiar male (negative 172control), and six experimental series of modified mate distance calls (in each series: calls played 173at natural rates, i.e., 2 calls.s-1; series broadcast at random; series duration: 10 seconds; interval 174between series: 30 seconds). 8 8
  • 9. 175 As the birds (recorded males, audience birds, and tested females) had been bred in the 176same aviary, all acoustic stimuli can be considered as perceptually equivalent for all of the birds. 177 1782.5. Playback experiments 179 1802.5.1. Experimental signals 181 182 A synthetic copy of one distance call (selected at random) of each recorded bird (n=6 183males, same individuals as those used for analysis) was created using the graphic synthesizer 184module of Avisoft-SAS Lab-Pro software (version 4.16, 2002). The copies were built to match as 185accurately as possible the acoustic characteristics of the original signals. As most of the energy in 186male distance calls is encompassed by seven harmonics in our population of zebra finches, all 187copies were synthesized with seven harmonics. These synthetic control copies were used to 188address the following questions. 189 1902.5.2. Do female zebra finches respond selectively to their mate voice? 191 192 To test the ability of female zebra finches to discriminate their mate among others, we 193played back to the females a series of 20 synthetic copies of male calls from their own mate and a 194series of 20 synthetic copies of calls from a familiar male. To rule out effects of particular 195individuals and limit the risk of pseudoreplication during playback experiments (McGregor et al., 1961992), each female was tested with calls from different familiar males. 9 9
  • 10. 197 1982.5.3. What are the acoustic cues used by the female for mate recognition? 199 200 In order to decipher how females identify a caller using the acoustic structure of its call, 201we used modified mate calls whose original characteristics were mixed with calls features of a 202familiar male. 203 204Modifications of the temporal structure: we replaced temporal elements of the mate call with 205those of a familiar male. The first experimental signal was built using the tonal component of the 206mate call associated with the downsweep component of the call of a familiar male (signals TM, 207Figure 2a) ; the second experimental signal was built using the tonal component of a familiar 208male call associated with the downsweep component of the mate call (signals TF, Figure 2a). 209Because the most individualized part of the male call is the downsweep component (see Results), 210we tested whether this part alone (signals DS, Figure 2a) is sufficient to evoke selective response 211from the female. All the following signal modifications concern this final downsweep component 212alone. For each modification, we chose to replace the initial mate call parameter by the same 213parameter measured in the call of a familiar male. 214 215Modification of the fundamental frequency: the fundamental frequency of the mate call was 216shifted to reach the mean values of fundamental frequency of the familiar male call (signals FF, 217Figure 2b). The natural amplitude envelope, the energy spectrum and temporal structures of the 218mate call remained unchanged. 219 10 10
  • 11. 220Modification of the frequency modulation: the slope of frequency modulation of the fundamental 221frequency of the mate call was modified to reach the slope of frequency modulation of the 222fundamental frequency of a familiar male call (signals FM), Figure 2b). The natural amplitude 223envelope, the energy spectrum and the natural mean fundamental frequency remained unchanged. 224 225Modification of the energy spectrum: the natural energy spectrum of the final downsweep 226component of the mate call was replaced with the energy spectrum of a familiar male call (signals 227ES, Figure 2b). The natural amplitude and frequency structures remained unchanged. 228 2292.6. Criteria of Response 230 231 During the playback test, the vocal and locomotor activity of the tested bird was 232monitored with a video recorder (SONY DCR-TRV24E). We measured the latency of the vocal 233response (LR in seconds) and the number of distance calls emitted during the broadcasting of the 234stimuli (NC). Prior to the beginning of playback broadcasting, we made sure that the bird 235spontaneous activity was low (no vocalizations emitted during the minute that preceeded the 236experiment). 237 2382.7. Statistical Analysis of playback experiments 239 240 When a female showed a shorter latency (LR) and/or a greater number of calls (NC) in 241response to mate calls than to familiar male calls, its response was considered as a mate 242recognition behaviour. To assess the effectiveness of mate call recognition by female zebra 11 11
  • 12. 243finches, the number of females showing a mate recognition behaviour was compared to the 244number of females showing no mate-directed behaviour using binomial test. 245 246 To assess the behavioural response to experimental (modified) signals and mate calls, we 247defined two ratios of reference: 1) the reference latency ratio = (LR in response to familiar 248calls) / (LR in response to mate calls); 2) the reference calling ratio = (NC in response to mate 249calls + 1) / (NC in response to familiar calls + 1). A mate recognition behaviour was expressed as 250follows: reference latency ratio + reference calling ratio e 2. For each tested modification and for 251each bird, we defined the two following ratios: 1) the latency ratio = (LR in response to modified 252calls) / (LR in response to mate calls); 2) the calling ratio = (NC in response to modified calls + 2531) / (NC in response to familiar calls + 1). These ratios were compared to the reference ratios. If 254latency ratio > reference latency ratio, the stimulus received 0 point, if latency ratio < reference 255latency ratio, the stimulus received 2 points, and if latency ratio < reference latency ratio but is 256bigger than one, the stimulus received 1 point. In case of no response to a stimulus, no point was 257assigned to this stimulus. If calling ratio > reference calling ratio, the stimulus received 2 point, if 258calling ratio < reference calling ratio, the stimulus received 0 point, and if calling ratio < 259reference calling ratio but is bigger than one, the stimulus received 1 point. In case of no 260response to a stimulus, no point was obtained by this stimulus. A stimulus was considered to 261induce a mate recognition behaviour if its total score was e 2. To compare the number of 262recognition responses obtained by modified calls with the number of recognition responses 263obtained by control mate calls, we used Wilcoxon paired-samples tests with a Bonferroni 264correction for multiple tests. 265 12 12
  • 13. 2663. Results 267 2683.1. Description of male calls and potential for individual identity coding 269 270 The fundamental frequency of the distance call of the male zebra finch has a mean start 271frequency of 730 Hz (Table 1), its short stable part (mean duration .018 s) presents a mean 272frequency between 827 and 1031 Hz, and its mean end frequency is of 509 Hz. Thus, the call is 273frequency modulated, with a mean ascending frequency modulation of the initial segment of 2743800 Hz.s-1 and a descending final segment with a mean frequency modulation of 5607 Hz.s-1. 275Most of the call energy is concentrated between 2000 and 4000 Hz (band 3 and 4) and the first 276peak of amplitude has a mean frequency of 2809 Hz. The call is amplitude modulated: the ratio 277RMSmax / RMS aver is different from 1. The highest peak of amplitude occurs during the final 278downsweep part. 279 As summarised in Table 1, all the measured parameters except dstab and Fmasc are 280significantly modified by the identity of the caller (Kruskal-Wallis ANOVA, p < .05). For all 281these parameters, the coefficients of variation within individuals are smaller than those among 282individuals: all the parameters except dstab and Fmasc are potential cues for individual identity 283coding. The PIC values of two frequency parameters are greater than 2: the frequency of the end 284of the stable part (Fstab2) and the slope of the descending frequency modulation (Fmdesc) are 285thus highly individualized. Three spectral parameters (bands 4, 5 and 6) present a PIC greater 286than 2: the energy spectrum of the call is thus well individualized. 287 The results of the multivariate approach also reveal an individual signature in the distance 288call of male zebra finches. Using the principal components calculated with the acoustic 13 13
  • 14. 289parameters showing a significant between-individuals variation, we performed a discriminant 290analysis that separate 100% of the calls of the six males. 291 2923.2. Playback experiments 293 2943.2.1. Female zebra finches respond selectively to mate voice 295 296 Females responded with shorter latency (individuals f1, f2, f3, f5 and f6, Table 2) and/or 297with more calls (individuals f1, f3, f4, f5 and f6, Table 2) to mate calls than to familiar male 298calls, thus showing a mate recognition behaviour (mean latency to mate calls = 1.56±2.4 s, mean 299latency to familiar calls = 5.69±6.08 s ; mean number of calls in response to mate calls = 3.7±2, 300mean number of calls in response to familiar calls = 2.2±2 ; two-tailed binomial test P=0.03). 301The responses of all of the six tested females verified that reference latency ratio + reference 302calling ratio e 2. 303 14 14
  • 15. 3043.2.2. Female recognition seems to be sensitive to frequency features alterations of mate call 305 306 Due to the small number of tested individuals, the results show only tendencies and are 307not supported by statistical validity (after Bonferroni corrections). Nevertheless, it appears that 308some of the modifications are likely to impair mate vocal recognition more deeply than others 309(Table 2). 310 The most reliable signals are those presenting temporal alterations. Four females among 311the six tested individuals showed a mate recognition behaviour in response to composite signals 312built using the association of the tonal component of the mate call and the final downsweep 313component of the call of a familiar male (signal TM) and three females recognized composite 314signals built using the association of the tonal component of a familiar male call and the final 315downsweep component of the mate call (signal TF). The final downsweep component alone 316(signal DS) elicited recognition response by four females among the six tested individuals. 317 Conversely, shifts of the fundamental frequency of the final downsweep component of the 318mate call (signal FF) elicited recognition response by only two females among the six tested 319individuals. Likewise, mate vocal recognition seems especially impaired when the frequency 320modulation or the energy spectrum of the mate call was replaced respectively by the frequency 321modulation or the energy spectrum of a familiar male call (signal FM). Indeed, only two females 322among the six tested individuals showed recognition responses in both situations. 323 3244. Discussion 325 3264.1. Acoustic features encoding individual signature in male distance calls 327 15 15
  • 16. 328 The analysis of the distance calls of male zebra finches highlights that some acoustic 329parameters are likely to be used as cues for individual identity coding. Particularly, frequency 330parameters of the fundamental frequency of the call - like the frequency of the end of the stable 331part (Fstab2) and the slope of the descending frequency modulation (Fmdesc) - as well as spectral 332parameters - like the band energy between 3000 and 6000 Hz - are highly individualized. 333Consequently, information about individual identity is likely to be encoded in both spectral 334domain and temporal pattern: the energy spectrum of the call as well as the temporal pattern of 335frequency modulation of the final downsweep part are good candidates for individual identity 336coding. Frequency modulation is known to support acoustic coding of information in several bird 337species (Jouventin et al., 1999; Lengagne et al., 2000; Mathevon and Aubin, 2001; Charrier et al., 3382001) but also in mammals (Charrier et al., 2002). 339 According to our analysis, some parameters are unlikely to encode individual identity. 340Temporal parameters like the duration of the stable part (dstab) or the slope of the ascending part 341of the call (Fmasc) are variable features both within individuals and among individuals. Such 342acoustic cues can not encode any information about the identity of the caller. 343 Consequently, we hypothesize that the acoustic parameters used by females to identify 344their mate may be characteristic of the well individualized final downsweep part of the call like 345(i) its frequency modulation, (ii) the absolute values of its fundamental frequency and (iii) its 346energy spectrum. 347 3484.2. Acoustic parameters used by female zebra finches for mate call recognition 349 350 Since only 6 females were tested and given the mixed results we obtained, it is difficult to 351sketch a precise picture of how females proceed to identify a caller. However, it remains possible 16 16
  • 17. 352to draw a general tendency. First, mate vocal recognition seems to remain possible even if a part 353of the call is absent or modified. Second, whereas mate recognition can be performed using the 354downsweep part alone, modifications of its frequency modulation, its energy spectrum, or the 355absolute values of its fundamental frequency are likely to impair the recognition process. Given 356these results and the data from call analysis, females could use both the energy spectrum and the 357slope of frequency modulation of the downsweep part to identify the call of their mate. The vocal 358signature is certainly multi-parametric, presenting a redundancy between tonal and downsweep 359parts that allows females to compensate the absence of segments by using the remaining 360information. Given the high temporal and frequency discrimination abilities of zebra finches 361(e.g., Weisman et al. 1998, Lee et al. 2006, Lohr et al. 2006, Friedrich et al. 2007), this vocal 362recognition system is likely to be efficient in spite of the noisy environment of the colony. 363 3644.3. A vocal signature participating in pair-bond maintenance 365 366 As proposed by some authors, the maintenance of long-lasting pair bonds could avoid the 367necessity for active, elaborate display before breeding and thus could allow reducing activity and 368energy expenditure in an unpredictable environment (Davies, 1982). This could provide an 369evolutionary explanation for monogamy in species of arid areas like the zebra finch. Monogamy 370could thus provide a ready-to-use reproductive system, which could rapidly start breeding after 371uncertain rainfall periods (Cynx, 2001). In such opportunistic species, there is thus a need for a 372bird to efficiently recognize its mate during and outside the breeding season. Particularly, 373nomadic species like the zebra finch need to perform mate recognition without site fidelity. Some 374previous studies report that whereas tactile contact between mates is necessary in the process of 375pair-formation, established pair-bonds can be maintained by auditory contact alone between 17 17
  • 18. 376mates (Silcox and Evans, 1982). Our results show that female zebra finches perform mate 377recognition using male calls. Nevertheless, it does not exclude that other sensory channels can be 378used for mate recognition, e.g., visual cues have been demonstrated to play a role in zebra finches 379pair bond maintenance (Butterfield, 1970). 380 381 382Acknowledgements 383 384We warmly thank Chris Sturdy for his welcome to contribute this modest paper in honour of Ron 385Weisman. This work was supported by the French National Research Agency (ANR, project 386‘BIRDS’VOICES’) and by the Program ‘Emergence’ of the Région Rhône-Alpes. NM is funded 387by the Institut universitaire de France (IUF). We are grateful to Colette Bouchut for technical 388assistance and Corinne Eyzac for taking care of the birds. Many thanks to Noémie Constant and 389Sébastien Tisseur for their help during the calls recording and analysis. 18 18
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  • 23. 470 Figures captions 471 472 Fig. 1. Acoustic structure of the distance call of a male zebra finch. (a) Spectrogram and 473oscillogram of the distance call. The distance call is composed of a fundamental frequency and 474several harmonics. It can be divided into a first segment (the Tonal component) composed by an 475initial rapid ascending frequency modulation of low amplitude followed by a short stable part, 476and a second segment defined by a long and loud descending frequency modulation (the 477Downsweep component). (b) Fundamental frequency of the call (obtained with the cepstrum 478method) used to describe the frequency modulation. We measured the duration of the ascending 479frequency modulation of the tonal component (dasc, s), the duration of the stable part of the tonal 480component (dstab, s), the duration of the descending frequency modulation of the downsweep 481component (ddesc, s), as well as the start frequency (Fstart, Hz), the frequency at the beginning 482of the stable part (Fstab1, Hz), the frequency at the end of the stable part (Fstab2, Hz), and the 483end frequency of the call (Fend, Hz). (c) Amplitude envelope of the call. The parameters 484measured were the mean intensity of the entire call (RMSaver, dB), the loudest intensity in the 485call (RMSmax, Pa) and the duration between the beginning of the call and the time at which the 486highest amplitude in the call occurs (Tmax, s). (d) Average power spectrum calculated from the 487total length of the call with the LPC method (linear predictive coding). The frequency of the first 488peak amplitude (Fmax, Hz) and the intensity of this peak (Imax, dB) were measured. 489 490Fig. 2. Spectrograms of a male distance call and experimental modified calls. (a) Control male 491call (mate call) and calls presenting modifications of their temporal structure. TM : the tonal 492component of the mate call is associated with the final downsweep component of the call of a 493familiar male. TF : the tonal component of a familiar male call is associated with the final 23 23
  • 24. 494downsweep component of the call of the mate. DS : the final downsweep component of the mate 495call is tested alone. (b) The final downsweep component (DS) of the mate call and its 496modifications in the frequency and the time domains. FF: shift of the fundamental frequency. 497FM: Modification of the frequency modulation. ES: Modification of the energy spectrum. 24 24
  • 27. 506 Standard PIC Kruskal-Wallis Variable Mean Mean CVi CVb Deviation CVb / mean CVi P value dstab (s) 0.018 0.006 36,5 33,61 0,92 p > .05 Tmax (s) 0.05465 0.02028 26,77 37,28 1,39 * Fstart (Hz) 730 25.1 2,77 3,47 1,25 * Fstab1 (Hz) 827 17 1,67 2,07 1,24 * Fstab2 (Hz) 1031 313.3 3,44 30,53 8,87 * Fend (Hz) 509 54 7,19 10,66 1,48 * Fmasc (Hz.s-1) 3800 845.5 22,46 22,44 1,00 p > .05 Fmdesc (Hz.s-1) 5607 1883 12,46 33,74 2,71 * RMSmax/ RMSaver 0.0056 0.0024 28,47 43,05 1,51 * Imax / RMSaver 0.741 0.0453 3,59 6,14 1,71 * Fmax (Hz) 2809 309.5 7,77 11,07 1,42 * Band1 (%) 0.29 0.29 61,51 100,45 1,63 * Band2 (%) 2.7 2.4 48,67 89,29 1,83 * Band3 (%) 37 21 41,71 57,01 1,37 * Band4 (%) 52 59 46 113,98 2,48 * Band5 (%) 17 38 58,92 224,55 3,81 * Band6 (%) 5.5 14 70,08 255,70 3,65 * 507 508 509Table 1 510Analysis of the individuality of the acoustic parameters of the male distance call. To describe the 511intra-individual and inter-individual variations of each parameter we used the coefficient of 512variation (CV) (Sokal & Rolhf, 1995). For each parameter we calculated CVi (within individual 513CV) and CVb (between individual CV). * corresponds to p < .05. Bold PIC values correspond to 514PIC > 2. 27 27
  • 28. 515 Total LR LR reference NC NC reference Total Total Total Total Total Total Tested score mate familiar latency mate familiar calling score score score score score score females of calls calls ratio calls calls ratio of TM of TF of DS of FF of MF of ES mate f1 0,356 1,579 4,43 5 2 2 2 3 1 2 0 0 0 f2 0,33 1,579 4,78 2 6 0,43 2 0 4 0 0 2 0 f3 1,705 16,59 9,73 1 0 2 2 0 3 3 0 1 1 f4 0,449 0,376 0,84 6 2 2,33 2 4 1 2 0 0 3 f5 0,172 6,446 37,48 5 1 3 2 2 2 2 2 2 2 f6 6,326 7,562 1,19 3 2 1,33 2 3 0 0 4 0 0 number of females performing mate 6 4 3 4 2 2 2 recognition P value 0.89 0.79 0.29 0.22 0.07 0.11 (Wilcoxon test) 516 517 518Table 2 519Responses of females to mate calls, familiar calls and modified mate calls. LR: latency of the 520vocal response (in seconds), NC: number of distance calls emitted during the broadcasting of the 521stimulus. 28 28