Biological Journal of the Linnean Society, 2009, 96, 115–134. With 6 figures

Acoustic convergence and divergence in two sympatric burrowing nocturnal seabirds CHARLOTTE CURE1,2*, THIERRY AUBIN1 and NICOLAS MATHEVON1,2 Equipe ‘Communications acoustiques’, Laboratoire de Neurobiologie, de l’Apprentissage, de la Mémoire et de la Communication UMR CNRS 8620, Université Paris-Sud, F-91405 Orsay cedex, France 2 Laboratoire d’Ecologie et Neuro-Ethologie Sensorielles EA3988, Université Jean Monnet, F-42023 Saint-Etienne cedex 2, France 1

Received 23 January 2008; accepted for publication 21 April 2008

Shearwaters are nocturnal burrowing seabirds. They return to their colony at dusk and exhibit high vocal activity, underlining the usefulness of acoustic cues to nocturnal communication. The present study aimed to test whether acoustic communication systems of two sympatric shearwater species, the Yelkouan shearwater Puffinus yelkouan and the Mediterranean Cory’s shearwater Calonectris diomedea diomedea, converge to similar strategies. Interannual mate fidelity and incubation relays led us to focus on sex and individual acoustic signatures. We first characterized those two signatures by analysing the major call emitted by incubating birds. Second, we performed playback experiments to assess ability of birds to vocally discriminate between sexes and mate versus non-mate. The results obtained show that both species use a reliable sex vocal signature supported by frequency and energy features, enabling sex identification of the emitter. By responding only to conspecific same-sex calls, birds may ensure burrow and mate guarding. Conversely, individual vocal signature was mainly supported by temporal parameters, and was more reliable in the Cory’s shearwater. Moreover, this species uses vocal exchanges to identify the mate during incubation relays, whereas Yelkouan shearwaters probably need additional cues. In conclusion, we observe an evolutionary convergence in intra-sex communication process but a divergence in mate greeting strategy. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134.

ADDITIONAL KEYWORDS: call signatures – communication strategy – mate identification – shearwaters –

vocal sex recognition.

INTRODUCTION Sender identity is one of the important messages coded by communication signals (e.g. animals may provide information about their species, sex, and individual identity, facilitating recognition at different levels). For example, it has been shown that numerous species of songbirds can discriminate and indicate preferences for their mates (Miller, 1979; Lind, Dabelsteen & McGregor, 1996; O’Loghlen & Beecher, 1997). As underlined in a recent review (Tibbetts & Dale, 2007), there are numerous potential benefits as well as costs associated with identity signalling. Various

*Corresponding author. E-mail: [email protected]

ecological (both environmental and social) constraints may thus drive the evolution of identity signaling. There is substantial evidence that environmental constraints influence the evolution of acoustic signals (Wiley & Richards, 1982; Mathevon et al., 2008). Some birds living in forest habitat have combined lower-pitched and narrower frequency range to broadcast species identity over long distances across dense vegetation (Slabbekoorn, 2004). In crowded and noisy seabird colonies, such as in penguins or gulls, an individual vocal signature allowing mate or parent– offspring recognition is encoded by a wide frequency spectrum and sharp amplitude modulations that facilitate sound localization, as well as a high redundancy that makes the signal efficient over the background noise generated by the colony (Aubin

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

115

116

C. CURE ET AL.

& Jouventin, 1998, 2002; Charrier et al., 2001; Jouventin & Aubin, 2002). Besides environmental constraints, social features may also modulate the encoding of vocal signatures. For example, previous studies on penguins and gulls showed that breeding system appears to constrain the sophistication of acoustic signature system (Lengagne, Jouventin & Aubin, 1999; Jouventin & Aubin, 2002; Mathevon, Charrier & Jouventin, 2003). From these penguin and gull studies, it appears that acoustic signalling of identity of colonial-nesting species highly depends on both environmental and social features. However, it is still unclear whether this observation can be extended to other colonial seabirds, which would support a general evolution rule. To test this, the present study focused on two sympatric shearwater species (belonging to the family Procellariidae) that bring a rare opportunity to compare their acoustic communication system. Procellariidae are monogamous species, breeding on seashores in large colonies of several thousands of individuals where background noise potentially constrains acoustic communication (Warham, 1990, 1996; Del Hoyo, Elliott & Sargatal, 1992). Moreover, whereas certain Procellariidae (e.g. fulmars) visit their colony by day and nest in the open, others such as shearwaters are nocturnal, vocalizing almost exclusively at night, and nest in burrows, two characteristics that reinforce the potential importance of acoustics due to an impaired visual communication, especially as shearwaters have poor nocturnal vision (Brooke & Prince, 1990; Warham, 1990; McNeil, Drapeau & Pierrotti, 1993). In addition, the combination of sexually monomorphic adult plumage and vocal greeting displays suggests that sound is likely to play a major role in mate recognition (Falls, 1982). The vocal repertoire of shearwaters typically includes a single major call and several minor calls (Bretagnolle, 1996). The major call is used for sexual (courtship and pair bond maintenance) and territorial (burrow defence) functions, whereas the minor calls are devoted to various other functions (begging, fighting, contact, copulation). Due to its biological roles, the major call may convey information related to both sex and individual identities of the sender. A sexual dimorphism has indeed been found in the major call of several shearwater species (Brooke, 1978, 1988; James & Robertson, 1985a) and may assure sexual advertisement in the dark. Furthermore, several elements support the idea that the major call could show an individual signature. Burrowing petrels indeed show inter-annual mate and nest site fidelity (Bradley et al., 1990; Thibault, 1994; Mougin et al., 1999; Mougin, 2000; Bried, Pontier & Jouventin, 2003) and perform regular incubation shifts implying mate recognition (Brooke, 1990; Bretagnolle, 1996).

To test whether similar environmental and social constraints can be linked to vocal signature systems in shearwaters, we studied the major call of two sympatric species: the Yelkouan shearwater Puffinus yelkouan, and the Mediterranean Cory’s shearwater Calonectris diomedea diomedea. Both species breed on the shores of the Mediterranean Sea, forming plurispecific colonies. In the absence of optical cues, due to their strictly nocturnal and fossorial habits, call and/or scent discrimination would be expected to occur between these two sympatric species, assuring reproductive isolation. To characterize sex and individual signatures, we analysed male and female major calls in both temporal and frequency domains. To assess the biological role of these signatures in the context of mate guarding and meeting, we tested: (1) sex vocal recognition by playing back same-sex calls and opposite-sex calls to both males and females and (2) individual recognition between mates by testing birds with mate calls versus non-mate calls. To identify adaptive convergences or divergences, we thus compared the acoustic system of both species, by analysing the acoustic structure of their respective major call and performing playback experiments.

MATERIAL AND METHODS STUDY

LOCATION AND ANIMALS

This study was conducted in 2005 and 2006 on mixed colonies of Yelkouan shearwaters (YS) and Mediterranean Cory’s shearwaters (CS) located on the shores of Port-Cros (43°00N, 6°23E) and Porquerolles (43°00N, 6°12E) Islands (Hyères archipelago, Mediterranean Sea). CS are heavier than YS (approximately 600 g for the former, Lo Valvo, 2001; and approximately 400 g for the latter, Bourgeois et al., 2007). Both species breed in burrows consisting of natural rock cavities in the cliffs. Although they breed in sympatric condition, the two species show different preferences in nest physical characteristics and do not appear to compete for the same burrows (Bourgeois & Vidal, 2007). CS start to prospect colonies in the middle of March, during the YS laying period. Fledging YS leave their nest in the middle of July, when eggs of CS start to hatch (Wink, Wink & Ristow, 1982; Thibault, 1985; Vidal, 1985; Bourgeois, 2006). Thus, breeding seasons of the two species overlap during several months. The field work was carried out during the respective incubation period of both species: March to May for YS and May to July for CS. Because pair mates took turns brooding the eggs every few days and were seldom simultaneously present at the nest, we were able to record and test males and females independently. Birds were sexed using

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS methods described in previous studies (Ristow & Wink, 1980; Bretagnolle & Thibault, 1995; Bourgeois et al., 2007). Recordings and playback experiments were performed at night between 21.00 h and 04.00 h, when birds were incubating in their burrows.

CALL

ANALYSIS

Modalities of call production In both species, birds vocalize in the nest, emitting series of four to five stereotyped burrow calls at a mean ± SD sound pressure level of 81.1 ± 2.1 dB for YS and 93.1 ± 1.2 dB for the CS (measured at a distance of 1 m from the beak with a 2235 Bruel and Kjaer decibel-meter set in microphone type 4176; N = 10 birds for each species with 4 ± 1 calls measured per individual). In shearwaters, sounds are produced during both the inhalation and the exhalation parts of the respiratory cycle (Warham, 1996). To determine the relationship between sounds and respiratory cycles, we observed the contraction and expansion of the thorax, throat and oral cavity by using an infrared JAMA camera mounted on a 1 m flexible handle. From the observation of the video recordings taken during calling activity of males and females in their burrows, inhalant and exhalant parts were then attributed to the corresponding sound structures represented on spectrograms. The call of CS is composed of four notes: two exhalant notes (EX1 and EX2) separated by a short breath (inhalant) note (IN1) and a longer one (IN2) (Bretagnolle & Lequette, 1990; Warham, 1996; Fig. 1). For YS, we showed in a previous study (Bourgeois et al., 2007) that the call is composed of two notes, a noisy note (harsher) and a clear one that shows visible harmonic series (Fig. 2). In this species, the note emitted during the exhalant phase of the respiratory cycle was correlated with the clear part of the male call but with the noisy part of the female call. Recordings and acoustic analysis Calls were recorded using a Sennheiser MKH70 microphone (frequency response: 30–20 000 Hz ± 1 dB) placed on the ground at the entrance of the burrow, and connected to a MARANTZ PMD 670 digital recorder (sampling frequency: 44.1 kHz). Recordings were resampled at 22 050 Hz and analysed with SYNTANA analytic package (Aubin, 1994) and Avisoft-SAS Lab Pro software, version 4.31 (Specht, 2004). We analysed 381 calls of YS (241 calls from 18 males and 140 calls from 12 females), and 206 calls of CS (104 calls from ten males and 102 calls from ten females). To describe the call structure, acoustic

117

variables were chosen in both temporal and frequency domains. The variables measured and their abbreviations are given in Table 1. Variables in the temporal domain were measured on amplitude envelopes (Figs 3C, 4E). Frequency variables describing energy spectral distribution were measured on energy spectra (Hamming window; FFTlength: 1024) (Figs 3A, B, 4A, B, C, D). Fundamental frequency values were tracked using autocorrelation, which is a method that allows the detection of periodical components in the signal (Randall & Tech, 1987) (Figs 3D, 4F). By following the autocorrelation curve of each note, we took values at regular intervals (50 values s-1) and then averaged them to obtain the mean frequency of the fundamental. To provide an accurate description of major calls of both species, we chose variables adapted to each call structure (Tables 2, 3). For each individual, the mean value of each acoustic parameter was calculated by averaging measurements made on its calls (mean number of analysed calls per individual: 12 ± 4 calls for YS and 11 ± 2 calls for CS). Each individual was therefore characterized by a set of 20 acoustic variables for YS and 45 for CS. Assessment of acoustic sexual signature The following analyses were performed separately for both species. To investigate call sexual dimorphism, a two-tailed t-test was applied to compare the mean individual value of each acoustic variable between sexes, after verifying the normality of data distribution. The variables that significantly differed between sexes were then used to perform a principal component analysis (PCA) to extract the acoustic features explaining the variability between sexes. To explain the variation, only the extracted factors with an eigenvalue greater than 1 were considered. A discriminant function analysis (DFA) based on all acoustic variables (20 in YS, and 45 in CS) was also performed. The principle of DFA is to maximize the ‘between groups’ variation and to minimize the ‘within group’ variation. Contrary to PCA, DFA separated groups with an a priori knowledge of the sex of the emitter. DFA provided a classification procedure that assigned each call to its appropriate group (correct assignment) or to an inappropriate one (incorrect assignment). To avoid sampling bias, we validated this classification by a Jackknife analysis (cross-validation; Lachenbruch & Mickey, 1968). Assessment of acoustic individual identity To test the individuality in male and female calls, four DFAs (one for each species and sex) were applied on 18 male and 12 female YS, and on ten males and ten female CS. Jackknife cross-validations were also

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

118

C. CURE ET AL. A

B

Figure 1. Spectrograms of a male (A) and a female (B) call of Cory’s shearwater. The call corresponds to two syllables, each of them being composed of two notes: an inhalant note (IN1 and IN2), and an exhalant one (EX1 and EX2).

applied to the classification procedures. To determine the acoustic variables potentially used to encode individual identity, we also calculated, for both species and both sexes, the coefficients of variation (CV) of each acoustic variable (Robinson, Aubin & Brémond, 1993). For each variable, we thus calculated the within-individual (CVi) and the inter-individual (CVb) CV using the formula (Scherrer, 1984): CV = 100 ¥ [1 + (1/4N)] ¥ SD/mean, where SD is the standard deviation, mean is the mean of the sample and N is the population sample. To assess the potential for individual coding (PIC) for each parameter, we calculated the ratio: PIC = CVb/mean CVi, where mean CVi is the mean value of the CVi of all the individuals. Parameters with a PIC value greater than 1 were interpreted as individual specific because their

within-individual variation is smaller than the interindividual variation. A one-way analysis of variance (ANOVA) was also used for each acoustic variable to assess differences among individuals. Because several acoustic features were measured on each call and multiple tests were performed on the same data set, we adjusted the significance level by using Bonferroni adjustment (Keppel, 1991).

PLAYBACK

EXPERIMENTS

Playback procedure Playback sessions were carried out on a sample of 15 females and 15 males for each species. Recorded calls were broadcast at the natural sound pressure levels (on average 80 dB for YS and 90 dB for CS) using a

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS

119

A

B

Figure 2. Spectrograms of a male call (A) and a female call (B) of Yelkouan shearwater. The call is composed of two parts: an inhalant note and an exhalant one.

MARANTZ PMD 690 connected to a loudspeaker (4 W) positioned at the entrance of the burrow. Because the studied species are nocturnal, playbacks of vocalizations can realistically simulate intrusions. All the birds tested occupied similar burrows of approximately 1 m in depth (Bourgeois & Vidal, 2007) and, for subsequent playback sessions, we kept the loudspeaker at the same distance from the bird. To test whether birds are able to identify: (1) the sex of the emitter and (2) their own mate from another bird of the same sex, each individual was tested once with three consecutive series of conspecific natural calls: (1) calls from a bird of the same sex (series A), (2) calls from a bird of the opposite sex (non-mate) (series B), and (3) calls from the mate (series C). Each series consisted of a natural recorded sequence of four calls repeated three times at an interval of 2 s (sequence duration of approximately 30 s). To prevent an effect of playback order on the results, the order of presentation of the three series was randomized. To avoid a possible bias due to cumulative excitation, we waited for at least 5 min of silence (duration between the stop of the broadcast

series and the end of the vocal response of the tested bird + 5 min during which bird remained silent) before applying the next playback series. To minimize pseudoreplication (McGregor et al., 1992), we used calls from different birds for both A and B series. As it has been recently shown that neighbour– stranger discrimination exists in another shearwater species (Puffinus l. lherminieri; Mackin, 2005), we never broadcast calls of immediate neighbours. Vocal response From the beginning of the playback experiment, vocal responses of the tested birds were recorded on a digital recorder. For each call series played back, the test period lasted 60 s (playback maximal duration: 30 s + corresponding additional time of observation). Preliminary tests and field observations showed that burrow-nesters vocally reply to conspecific calls by emitting series of calls, but do not reply to heterospecific calls of the sympatric species (C. Curé, unpubl. data). Consequently, during the playback session, we checked the presence/absence of vocal responses. When a vocal response occurred, the broadcast of the call series was interrupted to avoid harassment.

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

Exhalant note

EX

Inter-note silence duration Inter-call silence duration

INS ICS

Frequencies at the beginning, at the peak* and at the end of EX

Mean value of the fundamental frequency of EX

FBE, FPE, FEE

FoE

*Highest frequency value. †Lowest frequency value between the peak and the end of the note. ‡Lowest frequency value between the two peaks.

Energy spectral features FAmaxI Frequencies of maximum amplitude of IN F25%I, F50%I, Frequencies at the upper limit of the first (25%), F75%I second (50%) and third (75%) quartile of energy of IN FAmaxE Frequencies of maximum amplitude of EX F25%E, F50%E, Frequencies at the upper limit of the first (25%), F75%E second (50%) and third (75%) quartile of energy of EX

Mean value of the fundamental frequency of IN

FoI

Frequency analysis Fundamental frequency values FBI, FPI, FEI Frequencies at the beginning, at the peak* and at the end of IN

Duration of EX

DE

FAmaxE1, FAmaxE2 F25%E1, F50%E1, F75%E1, F25%E2, F50%E2, F75%E2

FAmaxI1, FAmaxI2 F25%I1, F50%I1, F75%I1, F25%I2, F50%I2, F75%I2

FBE1, FP1E1, FPLE1, FP2E1, FEE1 FBE2, FP1E2, FPLE2, FP2E2, FEE2 FoE1, FoE2

FoI1, FoI2

FBI2, FPI2, FPLI2, FEI2

FBI1, FPI1, FEI1

DI1 DI2 DE1 DE2 INS1 INS2 ISS ICS

EX2

IN1 IN2 EX1

Inhalant note

IN

Temporal analysis DI Duration of IN

Cory’s shearwaters

Yelkouan shearwaters

Frequencies of maximum amplitude of IN1 and IN2 Frequencies at the upper limit of the first (25%), second (50%) and third (75%) quartile of energy of IN1 and of IN2 Frequencies of maximum amplitude of EX1 and of EX2 Frequencies at the upper limit of the first (25%), second (50%) and third (75%) quartile of energy of EX1 and of EX2

Frequencies at the beginning, at the peak* and at the end of IN1 Frequencies at the beginning, at the peak*, at the plateau† and at the end of IN2 Mean value of the fundamental frequency of IN1 and of IN2 Frequencies at the beginning, at the first peak*, at the plateau‡, at the second peak*, and at the end of EX1. Frequencies at the beginning, at the first peak*, at the plateau‡, at the second peak*, and at the end EX2 Mean value of the fundamental frequency of EX1 and of EX2

Duration of IN1 Duration of IN2 Duration of EX1 Duration of EX2 Inter-note silence duration of first syllable Inter-note silence duration of the second syllable Inter-syllable silence duration Inter-call silence duration

Inhalant note of the first syllable Inhalant note of the second syllable Exhalant note of the first syllable Exhalant note of the second syllable

Table 1. Summary of abbreviations used to describe the calls of the Yelkouan and Cory’s shearwaters

120 C. CURE ET AL.

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS A

121

B

C

D

Figure 3. Acoustic variables measured on a female call of Yelkouan shearwater. Power spectrum of the inhalant note (A) and the exhalant note (B). C, envelope of the call showing the temporal variables. D, fundamental frequency detected by autocorrelation method. The frequency values measured on the fundamental frequency are shown for the inhalant and exhalant notes.

Behavioural responses to playback were also quantified by measuring on the recorded files the latency time elapsed between the beginning of the first played-back signal and the beginning of the first call emitted in reply by the tested individual. For each sex and for each species, the number of vocally responding individuals was compared between A and B series to assess whether birds can differentiate the gender of the emitter, and between B and C series to assess whether birds can discriminate their mate from another bird (two-tailed sign tests: P-value level set at P = 0.025 after applying Bonferroni correction). We did not take into account the latency time for these comparisons because the sample size of the

vocal responses to B series was too small to perform statistical tests. To assess whether CS respond differently to calls of the same sex and to calls of the mate, we compared latency time between A and C series using a t-test for dependant samples (P-value level set at P = 0.05). To test a possible sexual dimorphism in the vocal behaviour, the latency time to respond was compared between sexes for A series in both species, and for C series in CS only (because, for YS, the sample size of vocal responses was too small to perform this test) using a t-test for independent samples (P-value level set at P ! 0.05). To determine whether YS and CS show the same pattern of response to conspecific same-sex calls, the latency

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

122

C. CURE ET AL. A

B

C

D

E

F

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS

123

Figure 4. Acoustic variables measured on a male call of Cory’s shearwater. Power spectrum of the exhalant note of the first syllable (A), the inhalant note of the first syllable (B), the exhalant note of the second syllable (C), and the inhalant note of the second syllable (D). E, envelope of the call showing the temporal variables. F, fundamental frequency followed by autocorrelation method. The frequency values measured on the fundamental frequency are shown for the inhalant and exhalant notes of the two syllables. ! Table 2. Comparison between sexes of the 20 acoustic variables measured in Yelkouan shearwaters Males (N = 18) Variables ICS (s) INS (s) Inhalation DI (s) FBI (Hz) FPI (Hz) FEI (Hz) FoI (Hz) FAmaxI (Hz) F25%I (Hz) F50%I (Hz) F75%I (Hz) Exhalation DE (s) FBE (Hz) FPE (Hz) FEE (Hz) FoE (Hz) FAmaxE (Hz) F25%E (Hz) F50%E (Hz) F75%E (Hz)

Mean ± SD

Females (N = 12) Range

Mean ± SD

Range

t-values

0.09 ± 0.07 0.03 ± 0.01

0.02–0.26 0.01–0.05

0.03 ± 0.01 0.04 ± 0.01

0.02–0.04 0.01–0.06

-3.33** 1.78NS

0.87 ± 0.13 415.0 ± 46.2 566.5 ± 61.5 337.3 ± 42.9 448.6 ± 51.2 603.5 ± 222.9 490.8 ± 124.6 864.8 ± 334.6 1327.8 ± 417.5

0.63–1.04 343.1–504.3 434.5–679.1 256.3–433.0 360.6–561.3 360.8–1217.8 303.5–798.2 432.6–1479.5 615.5–2168.8

0.70 ± 0.12 350.4 ± 32.5 471.5 ± 31.6 314.3 ± 26.6 411.0 ± 19.6 436.6 ± 54.3 452.4 ± 56.4 957.6 ± 248.1 1867.8 ± 626.5

0.54–0.89 303.9–409.1 440.0–526.7 271.1–370.4 389.4–447.8 373.0–47.4 387.9–587.5 523.6–1338.1 1053.7–3115.6

-3.33** -4.19*** -4.91*** -1.65NS -2.41* -2.53* -1.00NS 0.82NS 2.84**

1.30 ± 0.21 539.2 ± 108.3 884.8 ± 56.8 430.4 ± 70.3 639.1 ± 48.8 983.1 ± 437.7 824.3 ± 312.0 1278.7 ± 456.9 2071.5 ± 632.7

0.95–1.75 398.3–710.7 745.2–953.4 320.5–561.0 534.4–725.7 491.7–1862.8 484.3–1540.8 654.5–2311.3 1053.0–3336.7

1.20 ± 0.25 350.5 ± 39.7 427.6 ± 32.6 325.1 ± 28.0 358.8 ± 24.4 501.0 ± 171.6 505.9 ± 126.7 1068.8 ± 416.1 1835.6 ± 659.5

0.90–1.73 280.3–413.2 370.8–463.2 282.9–366.1 308.7–397.0 297.1–805.0 323.8–732.1 545.4–2027.9 1033.5–3575.4

-0.98NS -5.75*** -25.16*** -4.91*** -18.36*** -3.62** -3.34* -1.28NS -0.98NS

t-test: *P < 0.05; **P < 0.01; ***P < 0.001; NS, not significant. For abbreviations, see Table 1.

time was compared for A series between species (separately for each sex), using a t-test for independent samples (P-value level set at P ! 0.05). All statistical tests were performed using STATISTICA, version 6.0 (StatSoft, 2001) and R software (Venables & Ripley, 2002; R Development Core Team, 2007).

RESULTS CALL

ANALYSIS

Sexual dimorphism In both shearwater species, the call of males and females could be differentiated on the basis of several variables in both frequency and temporal domains. The DFA applied on all acoustic variables extracted only 1 factor in both species (Yelkouan: Wilk’s l = 0.061, F20.360 = 276.609, P < 0.00001; Cory’s: Wilk’s

l = 0.0032, F45.160 = 1122.064, P < 0.00001) and classified 100% of the calls in the right gender (same results with cross-validation of Jackknife). The acoustical analysis showed that the mean values of 13 over the 20 acoustic variables in YS (Table 2) and 40 over the 45 in CS (Table 3) differed significantly between sexes. In the temporal domain, the ICS of YS was significantly higher in males than in females, whereas the INS did not differ between sexes. We obtained different results for CS since ISS, INS1, and INS2 were significantly higher in females than in males but ICS was not significantly different between sexes. Concerning the duration of each note, for both species, only the duration of the inhalant parts showed a significant sexual difference. In the frequency domain, almost all the measures related to the fundamental frequency were significantly higher in males than in females for both

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

124

C. CURE ET AL.

Table 3. Comparison between sexes of the 45 acoustic variables measured in Cory’s shearwaters Males (N = 10) Variables ICS (s) ISS (s) INS1 (s) INS2 (s) Exhalation 1 DE1 (s) FBE1 (Hz) FP1E1 (Hz) FPLE1 (Hz) FP2E1 (Hz) FEE1 (Hz) FoE1 (Hz) FAmaxE1 (Hz) F25%E1 (Hz) F50%E1 (Hz) F75%E1 (Hz) Inhalation 1 DI1 (s) FBI1 (Hz) FPI1 (Hz) FEI1 (Hz) FoI1 (Hz) FAmaxI1 (Hz) F25%I1 (Hz) F50%I1 (Hz) F75%I1 (Hz) Exhalation 2 DE2 (s) FBE2 (Hz) FP1E2 (Hz) FPLE2 (Hz) FP2E2 (Hz) FEE2 (Hz) FoE2 (Hz) FamaxE2 (Hz) F25%E2 (Hz) F50%E2 (Hz) F75%E2 (Hz) Inhalation 2 DI2 (s) FBI2 (Hz) FPI2 (Hz) FPLI2 (Hz) FEI2 (Hz) FoI2 (Hz) FAmaxI2 (Hz) F25%I2 (Hz) F50%I2 (Hz) F75%I2 (Hz)

Mean ± SD

Females (N = 10) Range

Mean ± SD

Range

t-values

0.15 ± 0.04 0.02 ± 0.01 0.01 ± 0.00 0.01 ± 0.00

0.11–0.24 0.01–0.04 0.01–0.02 0.01–0.02

0.16 ± 0.04 0.05 ± 0.03 0.02 ± 0.01 0.02 ± 0.00

0.10–0.24 0.01–0.09 0.01–0.04 0.01–0.02

0.78NS 2.48* 3.03** 2.62*

0.72 ± 0.09 352.5 ± 18.1 465.2 ± 23.5 400.8 ± 20.3 469.3 ± 23.7 343.1 ± 27.3 422.2 ± 19.5 509.4 ± 169.9 1081.9 ± 400.2 2948.6 ± 831.9 4927.4 ± 620.7

0.60–0.89 315.4–376.1 445.0–521.2 373.8–437.3 442.3–503.3 297.0–379.9 401.0–455.6 380.3–934.2 513.8–1729.6 1416.3–3755.7 3956.3–5817.9

0.76 ± 0.05 76.4 ± 9.7 87.4 ± 14.4 75.6 ± 11.8 88.7 ± 13.8 81.2 ± 11.9 78.2 ± 10.2 443.5 ± 77.2 420.9 ± 46.7 610.8 ± 85.9 1013.4 ± 361.4

0.67–0.85 56.6–92.9 61.9–110.9 52.9–93.5 66.2–111.1 60.2–100.2 58.1–95.6 379.6–649.9 360.0–498.8 494.7–717.0 638.2–1685.8

1.24NS -42.54*** -43.36*** -43.76*** -43.90*** -27.81*** -56.13*** -1.12NS -5.19*** -8.84*** -17.23***

0.09 ± 0.02 605.2 ± 75.2 668.8 ± 82.6 590.3 ± 65.2 627.9 ± 64.7 2157.7 ± 567.6 1934.4 ± 374.1 2837.1 ± 575.7 4184.2 ± 784.4

0.07–0.12 513.5–761.8 578.5–823.5 524.5–738.3 552.3–753.6 1351.0–3310.5 1283.3–2537.4 1634.4–3399.1 2662.0–5688.3

0.11 ± 0.02 226.6 ± 23.6 262.7 ± 31.6 215.1 ± 22.0 243.3 ± 27.5 510.2 ± 256.8 699.0 ± 255.4 1443.0 ± 493.0 2975.4 ± 1294.1

0.07–0.14 198.6–271.1 221.2–315.9 186.9–254.1 207.4–289.4 236.2–959.3 342.3–1122.8 968.3–2383.8 1377.0–5354.9

2.18* -15.19*** -14.52*** -17.26*** -17.30*** -8.36*** -8.62*** -5.81*** -2.53*

0.63 ± 0.08 322.0 ± 46.8 439.2 ± 23.4 389.5 ± 30.6 430.1 ± 30.4 335.9 ± 25.5 404.0 ± 22.0 970.9 ± 547.6 1404.7 ± 570.0 3146.2 ± 711.7 4932.0 ± 488.2

0.52–0.78 294.8–452.3 411.4–491.0 362.5–448.0 384.3–483.0 298.6–362.3 386.9–449.8 399.1–2089.7 738.6–2498.8 1890.5–3848.9 3916.0–5472.9

0.60 ± 0.10 72.0 ± 6.9 83.9 ± 9.1 73.7 ± 9.4 83.1 ± 10.5 76.8 ± 9.0 76.4 ± 8.0 567.8 ± 185.0 508.0 ± 135.0 742.7 ± 172.2 1457.4 ± 737.0

0.45–0.82 61.5–84.1 67.1–97.0 56.9–85.9 65.1–99.7 59.5–88.9 60.2–89.3 413.1–1030.8 405.0–847.6 552.2–1155.7 734.9–2918.8

-0.73NS -16.72*** -44.81*** -31.17*** -34.11*** -30.28*** -44.18*** -8.37*** -8.62*** -5.82*** -2.53*

0.48 ± 0.05 623.3 ± 73.5 738.8 ± 88.6 508.7 ± 63.4 632.7 ± 46.6 604.4 ± 55.0 2300.1 ± 538.6 1959.6 ± 407.5 2729.9 ± 428.9 3793.6 ± 393.4

0.41–0.54 545.2–769.0 641.7–926.4 422.9–636.8 570.7–728.8 514.3–710.2 1223.1–3233.0 1209.9–2726.6 1965.9–3449.6 3129.3–4481.0

0.39 ± 0.05 241.6 ± 21.9 291.4 ± 27.7 235.7 ± 20.0 269.3 ± 23.1 255.6 ± 26.5 330.7 ± 195.2 787.2 ± 379.7 1640.8 ± 608.8 3067.5 ± 1177.3

0.32–0.50 211.2–293.2 259.7–355.5 208.4–269.2 242.9–322.0 217.3–302.3 226.3–867.7 354.5–1599.9 853.7–2591.2 1534.4–5408.4

-3.69** -15.74*** -15.24*** -12.98*** -22.09*** -18.28*** -10.87*** -6.66*** -4.62*** -1.85NS

t-test: *P < 0.05; **P < 0.01; ***P < 0.001; NS, not significant. For abbreviations, see Table 1. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS A

Table 4. Principal component analyses (PCA) applied on acoustic features that significantly differed between sexes in male and female calls of Yelkouan and Cory’s shearwaters Variables

B

Figure 5. Principal component analysis. A, based on 13 acoustic variables and performed on Yelkouan shearwater’s calls (241 male calls and 140 female calls). B, based on 40 acoustic variables and performed on Cory’s shearwater’s calls (104 male calls and 102 female calls). Each dot corresponds to one call; black dots: male calls; white dots: female calls.

species and thus represent the most relevant parameters supporting sexual dimorphism. This is particularly obvious for the exhalant parts of the call that show no overlap between sexes for all the fundamental values in CS and for two variables (FPE and FoE) in YS. The majority of variables describing the energy spectrum (F50%E1, F75%E1, F50%E2, F75%E2, F25%I1, FAmaxI1, and FAmaxI2) were significantly higher in males than in females for CS with no overlap between sexes. For YS, three energy spectrum values (F25%E, FAmaxE, and FAmaxI) were higher in males than in females and one (F75%I) higher in females than in males. In both species, the PCA applied on acoustic parameters that significantly differed between sexes (13 for YS and 40 for CS) clearly separated the population calls in two groups corresponding to both sexes (Fig. 5A, B). Three factors with an eigenvalue greater than 1 were extracted from the PCAs and explained 66.4% and 83.9% of the variances, respectively, in YS and CS call samples (Table 4). In both species, all the fundamental frequency features of the call, especially

125

Factor 1

PCA on Yelkouan shearwaters ICS (s) 0.318 DI (s) 0.571 FBI (Hz) 0.702 FPI (Hz) 0.778 FoI (Hz) 0.681 0.436 FAmaxI (Hz) F75%I (Hz) -0.211 FBE (Hz) 0.794 FPE (Hz) 0.869 FEE (Hz) 0.692 FoE (Hz) 0.909 0.562 FAmaxE (Hz) F25%E (Hz) 0.566 Eigenvalues 5.55 Cumulative percentage 42.7 PCA on Cory’s shearwaters ISS (s) 0.392 INS1 (s) 0.508 INS2 (s) 0.475 DI1 (s) 0.355 DI2 (s) -0.670 FBE1 (Hz) -0.976 FP1E1 (Hz) -0.983 FPLE1 (Hz) -0.981 FP2E1 (Hz) -0.982 FEE1 (Hz) -0.969 FoE1 (Hz) -0.982 FBI1 (Hz) -0.958 FPI1 (Hz) -0.952 FEI1 (Hz) -0.956 FoI1 (Hz) -0.960 FBE2 (Hz) -0.949 FP1E2 (Hz) -0.979 FPLE2 (Hz) -0.976 FP2E2 (Hz) -0.979 FEE2 (Hz) -0.967 FoE2 (Hz) -0.980 FBI2 (Hz) -0.959 FPI2 (Hz) -0.954 FPLI2 (Hz) -0.902 FEI2 (Hz) -0.959 FoI2 (Hz) -0.954 F25%E1 (Hz) -0.649 F50%E1 (Hz) -0.871 F75%E1 (Hz) -0.937 -0.824 FAmaxI1 (Hz) F25%I1 (Hz) -0.866 F50%I1 (Hz) -0.791 F75%I1 (Hz) -0.515 -0.325 FAmaxE2 (Hz) F25%E2 (Hz) -0.686 F50%E2 (Hz) -0.909 F75%E2 (Hz) -0.901 -0.867 FAmaxI2 (Hz) F25%I2 (Hz) -0.840 F50%I2 (Hz) -0.706 Eigenvalues 29.30 Cumulative percentage 73.3

Factor 2

Factor 3

0.199 0.037 0.438 0.435 0.467 -0.198 -0.291 -0.093 -0.018 -0.240 -0.034 -0.622 -0.684 1.69 55.7

0.104 -0.399 0.310 0.265 0.446 0.229 0.702 -0.134 -0.296 -0.230 -0.241 0.241 0.215 1.40 66.4

0.518 -0.173 -0.207 0.301 0.041 -0.141 -0.126 -0.130 -0.130 -0.140 -0.132 -0.104 -0.121 -0.133 -0.122 -0.145 -0.140 -0.131 -0.123 -0.152 -0.135 -0.121 -0.118 -0.153 -0.131 -0.143 0.398 0.165 0.058 0.203 0.295 0.373 0.620 0.269 0.332 0.107 0.156 0.072 0.356 0.509 2.25 78.9

0.478 -0.541 -0.214 0.608 0.220 0.002 -0.004 -0.010 -0.019 0.039 -0.008 0.159 0.181 0.134 0.162 0.026 0.014 -0.005 -0.018 0.017 0.002 0.140 0.128 0.112 0.105 0.110 -0.425 -0.195 -0.055 -0.202 -0.093 0.025 0.245 -0.536 -0.425 -0.160 -0.032 -0.097 -0.045 0.051 2.00 83.9

Loadings of the variables are shown for the three first extracted factors. The most representative variables of each factor are marked in bold. For abbreviations, see Table 1.

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

126

C. CURE ET AL.

Table 5. Potential for individual coding of the 20 acoustic variables in males (241 calls from 18 males) and females (140 calls from 12 females) Yelkouan shearwaters Males (N = 18)

Females (N = 12) ANOVA

Variables

Mean CVi ± SD

CVb

ICS (s) INS (s) Inhalation DI (s) FBI (Hz) FPI (Hz) FEI (Hz) FoI (Hz) FAmaxI (Hz) F25%I (Hz) F50%I (Hz) F75%I (Hz) Exhalation DE (s) FBE (Hz) FPE (Hz) FEE (Hz) FoE (Hz) FAmaxE (Hz) F25%E (Hz) F50%E (Hz) F75%E (Hz)

76.19 ± 53.91 39.23 ± 21.11

73.23 33.52

5.38 ± 1.26 11.11 ± 4.65 8.71 ± 4.94 9.67 ± 5.38 6.44 ± 2.73 36.42 ± 22.63 16.09 ± 9.08 16.32 ± 9.05 19.69 ± 15.34

14.80 11.28 11.01 12.89 11.58 37.45 25.73 39.23 31.88

7.30 ± 1.57 13.19 ± 4.63 7.55 ± 3.63 6.79 ± 2.85 7.72 ± 3.55 10.93 ± 3.64 5.75 ± 1.71 32.29 ± 19.51 16.71 ± 8.64

16.46 20.37 6.51 6.54 9.89 16.56 7.74 45.14 38.38

ANOVA PIC

Mean CVi ± SD

CVb

0.96 0.85

37.93 ± 7.69 42.09 ± 20.39

23.04 32.92

4.375** 3.863**

0.61 0.78

64.41* 11.63* 18.68* 17.15** 41.15** 7.13** 28.61** 67.18* 39.95*

2.75 1.02 1.26 1.33 1.80 1.03 1.60 2.40 1.62

4.68 ± 2.37 9.68 ± 4.71 5.92 ± 2.86 6.90 ± 3.17 8.33 ± 9.47 28.31 ± 26.14 20.31 ± 12.39 32.25 ± 11.85 27.48 ± 19.70

17.97 9.46 6.84 8.65 4.60 13.26 13.05 26.94 35.14

136.7* 10.7** 13.26** 16.74* 8.482** 1.284NS 3.828** 10.93** 4.86**

3.84 0.98 1.15 1.25 0.55 0.47 0.64 0.84 1.28

66.92* 33.74** 6.839** 29.78* 23.3* 16.9** 70.13** 32.07* 15.17*

2.26 1.54 0.86 0.96 1.28 1.52 1.35 1.40 2.30

6.40 ± 2.21 9.57 ± 3.40 9.75 ± 3.78 10.02 ± 3.88 8.20 ± 9.07 47.12 ± 33.06 14.55 ± 6.96 20.91 ± 9.84 22.43 ± 10.56

21.06 11.56 7.79 8.79 6.13 34.12 25.57 39.99 36.91

97.87* 15.73* 7.185** 7.962** 16.71* 2.738* 23.73* 25.41* 31.0*

3.29 1.21 0.80 0.88 0.75 0.72 1.76 1.91 1.65

F-value 2.66* 7.672**

F-value

PIC

CVi, within-individual coefficient of variation; CVb, between-individual coefficient of variation; PIC, potential for individual coding (= CVb/CVi). P-values are Bonferroni adjusted. *P < 0.05; **P < 0.01. NS, not significant. ANOVA, analysis of variance. For abbreviations, see Table 1.

those of the exhalant notes, were the most representative variables of the first factor which contributed to 42.7% and 73.3% of the variance in YS and CS respectively. Moreover, in CS, the great majority of energy features, particularly those of the exhalant notes, were strongly correlated with the first factor. In YS, energy features of the exhalant note (FAmaxE and F25%E) appeared also relevant since they represented the variables contributing the most to the second factor, which explained 13% of the variance. In CS, the second factor explained only 5.7% of the variance and was represented by one parameter of the energy spectrum (F75%I1) and one temporal feature (ISS). In conclusion, fundamental frequency and energy features of the exhalant notes were the most sexually dimorphic variables in both species. Individual identity According to our analysis, calls did present features linked to individual identity in both species. However,

it appeared that individual signature was more pronounced and reliable in CS calls than in those of YS. In both shearwater species and for both sexes, each acoustic variable showed a significant difference among individuals, except for one parameter (FAmaxI) in female YS (ANOVA; Table 5), and two parameters (FAmaxE1 and F75%E2) in male CS (ANOVA; Table 6). PCI results showed that many call features participated in the individual signature in both species (variables with PCI > 1). For a given variable, when PIC value was above 2, the variable was considered as highly individualized. A common result in both species and both sexes is that note durations (DI and DE for YS; DE2 for CS) are the variables showing the highest PIC values (Tables 5, 6). The individual signature appeared to be more relevant in CS than in YS because the greatest PIC values obtained for the former were much higher than those obtained for the latter. Moreover, although the variables showing

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS

127

Table 6. Potential for individual coding of the 45 acoustic variables in males (104 calls from ten males) and females (102 calls from ten females) Cory’s shearwaters Males (N = 10)

Females (N = 10) ANOVA

ANOVA PIC

Mean CVi ± SD

CVb

F-value

PIC

84.48* 38.43* 15.56** 21.51*

3.59 2.17 1.31 1.92

5.98 ± 1.93 32.19 ± 14.24 30.77 ± 9.68 28.00 ± 8.31

23.68 58.21 35.07 22.23

111.3* 33.56* 13.09** 4.741**

3.96 1.75 1.14 0.79

12.51 5.27 5.18 5.20 5.18 8.15 4.72 34.18 37.92 28.92 12.91

32.36* 6.378** 13.85** 18.24* 23.56* 8.569** 17.62** 2.247NS 4.72** 9.055** 4.501**

2.14 0.81 1.23 1.33 1.56 0.95 1.31 1.19 0.82 0.83 0.69

4.81 ± 2.17 11.96 ± 5.26 11.37 ± 4.69 10.91 ± 4.52 11.66 ± 4.11 13.00 ± 4.05 10.40 ± 5.34 15.21 ± 9.85 10.00 ± 4.63 12.65 ± 4.40 26.96 ± 21.73

6.81 12.97 16.88 15.99 15.90 15.07 13.38 17.84 11.36 14.42 36.55

15.59** 9.179** 13.54** 13.86** 11.77** 8.793** 12.28** 9.971** 10.13** 12.55** 6.18**

1.42 1.08 1.49 1.47 1.36 1.16 1.29 1.17 1.14 1.14 1.36

9.77 ± 4.48 6.64 ± 2.86 5.81 ± 2.95 7.13 ± 3.09 8.51 ± 3.16 34.24 ± 9.69 22.87 ± 6.74 20.62 ± 7.16 20.85 ± 12.98

24.61 12.74 12.66 11.31 10.56 26.96 19.82 20.80 19.22

14.96** 36.88* 43.54* 25.35* 55.83* 5.976** 6.364** 10.76** 6.054**

2.52 1.92 2.18 1.59 1.24 0.79 0.87 1.01 0.92

11.66 ± 6.59 6.34 ± 8.04 6.31 ± 8.33 8.22 ± 9.72 3.72 ± 1.68 52.84 ± 36.09 27.81 ± 16.95 23.47 ± 10.80 30.61 ± 23.10

16.86 10.66 12.32 10.47 11.58 51.59 37.42 35.02 44.58

15.61** 14.42** 15.38** 8.174** 83.3* 5.483** 11.62** 14.6** 20.46*

1.45 1.68 1.95 1.27 3.11 0.98 1.35 1.49 1.46

2.96 ± 0.81 7.94 ± 4.11 3.55 ± 1.09 3.66 ± 1.37 3.01 ± 1.23 6.98 ± 2.77 3.83 ± 2.00 56.50 ± 37.20 39.33 ± 15.43 25.56 ± 20.60 17.49 ± 7.98

13.28 14.89 5.46 8.06 7.25 7.79 5.59 57.81 41.59 23.19 10.15

176.8* 22.7* 21.21* 46.97* 55.06* 11.75** 36.34* 4.305** 7.623** 8.935** 2.654NS

4.49 1.88 1.54 2.21 2.41 1.12 1.46 0.60 0.63 0.85 2.97

4.09 ± 2.43 11.43 ± 2.50 11.07 ± 2.65 9.86 ± 3.41 9.46 ± 3.97 10.17 ± 3.54 9.45 ± 4.00 26.75 ± 11.77 13.91 ± 7.70 11.30 ± 4.25 29.56 ± 22.54

17.44 9.78 11.07 13.03 12.90 12.05 10.80 33.39 27.24 23.77 51.83

105.2* 7.433** 8.782** 14.06** 14.85** 11.31** 11.48** 12.26** 34.04* 43.25* 12.8**

4.26 0.86 1.00 1.32 1.36 1.19 1.14 1.25 1.96 2.10 1.75

4.94 ± 3.38 6.24 ± 2.87 7.63 ± 3.68 13.73 ± 5.78 7.06 ± 4.39 9.44 ± 3.65 31.58 ± 13.25 19.22 ± 7.35 18.25 ± 6.20 14.05 ± 5.78

11.09 12.09 12.29 12.78 7.55 9.32 24.00 21.32 16.10 10.63

33.76* 34.41* 25.53* 8.893** 9.435** 19.26* 5.033** 10.63** 7.874** 5.718**

2.25 1.94 1.61 0.93 1.07 0.99 0.76 1.11 0.88 0.76

4.90 ± 1.28 4.79 ± 1.24 3.90 ± 0.87 5.88 ± 1.52 3.23 ± 1.06 6.18 ± 7.72 30.05 ± 39.57 31.82 ± 20.50 27.61 ± 14.96 25.81 ± 13.18

14.18 9.27 9.73 8.70 8.80 10.62 60.50 49.44 38.03 39.34

67.55* 56.73* 92.76* 27.08* 115.7* 16.42** 5.672** 16.07** 13.61** 23.07*

2.90 1.94 2.50 1.48 2.73 1.72 2.01 1.55 1.38 1.52

Variables

Mean CVi ± SD

CVb

ICS (s) ISS (s) INS1 (s) INS2 (s) Exhalation 1 DE1 (s) FBE1 (Hz) FP1E1 (Hz) FPLE1 (Hz) FP2E1 (Hz) FEE1 (Hz) FoE1 (Hz) FAmaxE1 (Hz) F25%E1 (Hz) F50%E1 (Hz) F75%E1 (Hz) Inhalation 1 DI1 (s) FBI1 (Hz) FPI1 (Hz) FEI1 (Hz) FoI1 (Hz) FAmaxI1 (Hz) F25%I1 (Hz) F50%I1 (Hz) F75%I1 (Hz) Exhalation 2 DE2 (s) FBE2 (Hz) FP1E2 (Hz) FPLE2 (Hz) FP2E2 (Hz) FEE2 (Hz) FoE2 (Hz) FAmaxE2 (Hz) F25%E2 (Hz) F50%E2 (Hz) F75%E2 (Hz) Inhalation 2 DI2 (s) FBI2 (Hz) FPI2 (Hz) FPLI2 (Hz) FEI2 (Hz) FoI2 (Hz) FAmaxI2 (Hz) F25%I2 (Hz) F50%I2 (Hz) F75%I2 (Hz)

8.07 ± 3.88 22.94 ± 11.52 23.67 ± 9.75 20.84 ± 5.92

28.97 49.80 31.00 39.97

5.85 ± 4.68 6.51 ± 2.55 4.20 ± 1.32 3.90 ± 0.77 3.32 ± 1.16 8.57 ± 3.76 3.60 ± 0.88 28.75 ± 36.44 46.49 ± 13.95 34.88 ± 25.57 18.61 ± 7.75

F-value

CVi, within-individual coefficient of variation; CVb, between-individual coefficient of variation; PIC, potential for individual coding (= CVb/CVi). P-values are Bonferroni adjusted. *P < 0.05; **P < 0.01. NS, not significant. ANOVA, analysis of variance. For abbreviations, see Table 1. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

128

C. CURE ET AL. A

B

C

D

Figure 6. Discriminant function analyses applied to the 20 acoustic variables measured in Yelkouan shearwaters (A, B) and to the 45 acoustic variables measured in Cory’s shearwaters (C, D). A, 241 calls from 18 males. B, 140 calls from 12 females. C, 104 calls from ten males. D, 102 calls from ten females. On this basis, 91% (A), 90% (B), 98% (C), and 97% (D) of the calls, were correctly classified (cross-validation of Jackknife) in the right individual call group. Each dot corresponds to one call; each sign corresponds to one individual call group.

a high potential of individuality concerned almost exclusively note durations in YS, it concerned many other features (duration parameters but also fundamental frequency values and energy distribution) in CS. The four DFAs applied separately on each sex of each species indicated that a great majority of variables are significantly different among individuals (YS: Wilk’s l = 0.000001, F340.270 = 14.778, P < 0.0001, for males, and Wilk’s l = 0.00001, F220.11 = 11.239, P < 0.0001, for females; CS: Wilk’s l = 0.0000001, F405.465 = 17.914, P < 0.0001, for males, and Wilk’s l = 0.000001, F405.447 = 18.468, P < 0.0001, for females). Cross-validation of Jackknife yielded an average correct classification of the calls in the right individual group of 91% (range = 60–100%) for male

YS, 90% (range = 67–100%) for female YS, 98% (range = 88–100%) for male CS, and 97% (range = 89– 100%) for female CS. Moreover, graphical representations of the calls obtained with the two first extracted factors of the DFA showed that, in both sexes, dots corresponding to calls of a given individual are more concentrated for the CS (Fig. 6C, D), indicating a low within-individual variation of acoustic features, than for the YS (Fig. 6A, B). The two first factors extracted from the DFAs explained the following proportion of the call variances: 54.0% for male YS, 64.9% for female YS, 62.9% for male CS, and 59.7% for female CS (Table 7). In males of both species, the most representative variables of the first factor (explaining 31.9% and 47.7% of the variance in YS and CS, respectively) were in

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS Table 7. Discriminant function analyses applied to calls of Yelkouan and Cory’s shearwaters

Variables

DFA on males

DFA on females

Factor 1

Factor 1

Factor 2

0.075 -0.086

-0.193 0.140

0.966 0.604 0.614 0.334 0.492 0.093 -0.002 0.052 0.120

-0.096 0.019 0.189 -0.034 0.011 -0.019 -0.091 -0.395 -0.257

0.859 0.258 0.108 0.229 0.279 -0.047 -0.061 0.120 0.138 17.25 47.6

0.385 -0.040 -0.201 -0.385 -0.471 -0.159 -0.752 -0.790 -0.800 6.90 64.9

0.685 -0.226 0.472 0.160

0.510 -0.266 0.036 0.179

0.137 0.013 0.074 0.040 0.097 -0.001 0.070 -0.035 0.187 0.263 0.034

-0.056 -0.359 -0.343 -0.403 -0.397 -0.376 -0.393 0.411 -0.023 -0.122 -0.378

-0.248 -0.539 -0.604 -0.490 -0.678 0.351 0.131

-0.452 -0.278 -0.143 -0.045 -0.234 -0.033 -0.321

Factor 2

DFAs on Yelkouan shearwaters ICS (s) 0.062 0.170 INS (s) -0.029 -0.187 Inhalation DI (s) 0.284 -0.719 FBI (Hz) 0.111 0.484 FPI (Hz) 0.140 0.320 FEI (Hz) 0.228 0.361 FoI (Hz) 0.168 0.560 FAmaxI (Hz) 0.420 0.247 F25%I (Hz) 0.609 0.443 F50%I (Hz) 0.738 0.500 F75%I (Hz) 0.531 0.511 Exhalation DE (s) 0.681 -0.551 FBE (Hz) 0.509 0.064 FPE (Hz) 0.171 -0.152 FEE (Hz) 0.690 -0.157 FoE (Hz) 0.372 0.126 FAmaxE (Hz) 0.582 0.321 F25%E (Hz) 0.698 0.290 F50%E (Hz) 0.592 0.327 F75%E (Hz) 0.262 0.048 Eigenvalues 12.42 8.77 Cumulative 31.9 54.0 percentage DFAs on Cory’s shearwaters ICS (s) -0.518 0.421 ISS (s) 0.529 0.384 INS1 (s) -0.117 -0.399 INS2 (s) -0.036 -0.418 Exhalation 1 DE1 (s) 0.507 0.506 FBE1 (Hz) -0.180 0.028 FP1E1 (Hz) -0.446 0.140 FPLE1 (Hz) -0.611 0.091 FP2E1 (Hz) -0.429 0.009 FEE1 (Hz) -0.162 0.323 FoE1 (Hz) -0.555 0.124 FAmaxE1 (Hz) 0.043 0.078 F25%E1 (Hz) -0.120 0.119 F50%E1 (Hz) 0.065 0.236 F75%E1 (Hz) -0.059 -0.006 Inhalation 1 DI1 (s) 0.123 0.480 FBI1 (Hz) 0.473 0.619 FPI1 (Hz) 0.431 0.657 FEI1 (Hz) 0.417 0.519 FoI1 (Hz) 0.479 0.607 FAmaxI1 (Hz) -0.039 0.246 F25%I1 (Hz) 0.001 0.288

129

Table 7. Continued

DFA on males

DFA on females

Variables

Factor 1

Factor 1

Factor 2

F50%I1 (Hz) F75%I1 (Hz) Exhalation 2 DE2 (s) FBE2 (Hz) FP1E2 (Hz) FPLE2 (Hz) FP2E2 (Hz) FEE2 (Hz) FoE2 (Hz) FAmaxE2 (Hz) F25%E2 (Hz) F50%E2 (Hz) F75%E2 (Hz) Inhalation 2 DI2 (s) FBI2 (Hz) FPI2 (Hz) FPLI2 (Hz) FEI2 (Hz) FoI2 (Hz) FAmaxI2 (Hz) F25%I2 (Hz) F50%I2 (Hz) F75%I2 (Hz) Eigenvalues Cumulative percentage

-0.045 -0.076

0.312 0.346

0.082 -0.199

-0.196 -0.388

0.900 -0.296 -0.361 -0.733 -0.746 -0.401 -0.658 -0.003 -0.149 -0.037 -0.190

-0.031 0.058 0.168 0.157 0.035 0.141 0.142 -0.020 0.147 0.266 0.056

0.769 0.071 0.128 0.054 0.146 0.041 0.030 0.581 0.681 0.675 0.213

-0.465 -0.419 -0.448 -0.600 -0.508 -0.491 -0.529 -0.208 -0.327 -0.381 -0.233

0.070 0.475 0.458 0.426 0.407 0.491 0.140 0.126 0.223 0.058 95.10 47.7

0.774 0.564 0.422 0.225 0.125 0.321 0.220 0.348 0.204 0.219 30.88 62.9

-0.248 -0.305 -0.472 -0.500 -0.684 -0.415 0.443 0.074 0.026 -0.073 91.7 37.9

-0.442 -0.580 -0.464 -0.137 -0.394 -0.269 -0.241 -0.432 -0.309 -0.416 53.30 59.7

Factor 2

In each case, discriminant function analysis was applied to male and female calls. Loadings of the variables are shown for the two first extracted factors. The most representative variables of each factor are marked in bold. For abbreviations, see Table 1.

the temporal domain the duration of the exhalant parts of the calls. In CS, the silence durations between calls or syllables were also more strongly correlated to the first factor. In the frequency domain, features of the energy spectrum were strongly related to the first factor in YS, whereas it concerned some fundamental frequency values of the second exhalant part in CS. The second factor (explaining 22.1% and 15.2% of the variance in YS and CS, respectively) was mainly represented by the duration of the inhalant parts of the calls in both species and, in CS only, by some fundamental frequency values of the inhalant parts. In females, the first factor (explaining 47.6% and 37.9% of the variance in YS and CS, respectively)

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

130

C. CURE ET AL.

Table 8. Vocal responses of Cory’s and Yelkouan shearwaters to different series of playback experiments Call series

A (same sex)

B (non-mate)

C (mate)

P

Vocal responses

Yes

No

Yes

No

Yes

No

A versus B

B versus C

15 15 15 15

0 0 0 0

0 4 0 0

15 11 15 15

4 3 13 14

11 12 2 1

0.0006*** 0.0006*** 0.0006*** 0.0051**

0.0017** 0.0010** 0.2672NS 1.0000NS

Yelkouan shearwaters Cory’s shearwaters

Females Males Females Males

Two-tailed sign test: P-value levels are Bonferroni corrected and set at: *P < 0.025; **P < 0.005; ***P < 0.0005. NS, not significant.

was essentially represented by note durations and fundamental frequency features of the inhalant parts. In CS, some energy spectrum features of the second exhalant note were also strongly correlated to the first factor. The second factor (explaining 17.4% and 21.8% of the variance in YS and CS, respectively) was mainly linked to energy spectrum features of the exhalant note in YS, whereas it was more related to the fundamental frequency values of the second exhalant note in CS.

PLAYBACK

EXPERIMENTS

Because each bird was tested with three call series, we first verified that no order effect existed (Friedman ANOVA: YS: c2 = 1.00, N = 15, d.f. = 2, P < 0.606 for males and c2 = 0.133, N = 15, d.f. = 2, P < 0.935 for females; CS: c2 = 0.421, N = 15, d.f. = 2, P < 0.810 for males and c2 = 0.571, N = 15, d.f. = 2, P < 0.751 for females). Sex discrimination: a response linked to call sex in both shearwater species In both studied species, the vocal response to calls played-back is sex-linked: whereas both males and females always responded to individuals of the same sex, almost no birds (except four males out of 15 YS) replied to the vocalizations of the opposite sex (A series versus B series; Table 8). Moreover, there is no significant difference in the latency time to reply to calls of the same sex (A series) between males and females (latency times: 8.3 ± 2.4 s for males versus 10.3 ± 5.1 s for females in YS, t = 1.42, P = 0.166, N = 15; 16.4 ± 4.7 s for males versus 19.4 ± 7.3 s for females in CS, t = -1.34, P = 0.192, N = 15). It can be noted that YS reply more quickly than CS to conspecific same-sex calls (YS versus CS: t = 5.97, P = 0.000002 for males; t = 3.97, P = 0.000206 for females). Mate–non-mate discrimination: a stronger response to mate voice in Cory’s than in Yelkouan shearwaters In YS, only a few individuals responded to mate voice (four out of the 15 tested females and three out of the

15 tested males; Table 8). It can be noted that, among those birds, all females but only two males replied exclusively to their mate. Three others called in reply only to non-mate calls, and only one of the males reacting to female calls responded to both mate and non-mate calls. Conversely, almost all CS (14 males and 13 females over the 15 tested in each sex; Table 8) responded to their mate’s calls whereas non-mate calls never elicited a vocal response. Among birds that responded to their mate (C series), no sexual difference was found in the response latency (males: 9.8 ± 4.9 s versus females: 9.1 ± 3.8 s, t = 0.43, P = 0.669, N = 14 males and N = 13 females). Moreover, for both sexes, the latency time was approximately two-fold shorter with mate calls than with same-sex calls (males: 9.8 ± 4.9 s for C series versus 16.4 ± 4.7 s for A series, t = -5.88, P = 0.000054, N = 14; females: 9.1 ± 3.8 s for C series versus 19.4 ± 7.2 s for A series, t = -5.25, P = 0.0.000206, N = 13).

DISCUSSION SEX

VOCAL SIGNATURE: A CONVERGENCE IN CALL

STRUCTURE AND FUNCTION BETWEEN YELKOUAN AND CORY’S SHEARWATERS

The major call of both shearwater species showed a reliable and well defined sex vocal signature. For each species, the PCA clearly separated recorded calls of the population into two groups, revealing a pronounced sexual dimorphism. Moreover, crossvalidations of Jackknife classified the calls in the correct gender with 100% accuracy. Call analyses enabled the extraction of key variables supporting evidence for sexual dimorphism in both species. In the temporal domain, only the duration of the inhalant parts was dimorphic. In YS, the duration of the inhalant note was longer in males than in females, making calls of males longer than those of females. In CS, the duration of the first inhalant part was longer in females, whereas the duration of the second inhalant part was longer in

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS males, making the duration of the whole call equal between sexes. Sexes also differed in the call emission rate. In YS, the silence interval between calls was shorter in females, implying that they call at a faster rate than males. Conversely, in CS, females tended to call at a slower rate than males, with the silences between notes and syllables being slightly longer in females. Such a dimorphism of temporal parameters between sexes has been also documented in other species of petrels and shearwaters (the Bulwer’s petrel Bulweria bulwerii: James & Robertson, 1985b; the Greater shearwater Puffinus gravis: Brooke, 1988; the Swinhoe’s storm-petrel Oceanodroma monhoris: Taoka & Okumura, 1990). In the frequency domain, male calls were higher pitched than female calls for both species. Moreover, fundamental frequency values were the most relevant parameters supporting the sexual dimorphism. This was particularly obvious for the fundamental frequency of exhalant parts with a value two- and five-fold higher in males than in females for YS and CS calls, respectively. Higher pitched calls in males than in females appears to be a common characteristic in petrels as this has been also reported for other shearwaters, such as the Manx shearwater (Puffinus puffinus; Brooke, 1978), and other petrels such as the Leach’s storm-petrel (Oceanodroma leucorhoa; Taoka et al., 1989a). Call pitch value is known to be susceptible to reflect the size or weight of individuals in numerous species, with lower values being associated with bigger size (Wallschläger, 1980; Fletcher, 2004). Thus, YS and CS constitute an exception to the rule, since males are slightly larger than females (Lo Valvo, 2001; Bourgeois et al., 2007). The distribution of energy among the frequency spectrum represents another cue that strongly differentiates males and females in both studied species. There was more energy on lower harmonics in females than in males, producing a timbre difference between sexes. Moreover, in CS, the slow amplitude modulation of the exhalant notes of females (periodic amplitude fluctuations: 14.1 ± 2.0 Hz for EX1; 14.5 ± 1.6 Hz for EX2) lead to the emission of rasping sounds, harsher than male ones. Finally, the exhalant note of YS call corresponded to the clear part in males but to the noisy part in females. This sexual dimorphism in the global structure of the vocalizations allowed us to hypothesize the existence of morphological differences between sexes in the vocal apparatus. Playback tests demonstrated that YS and CS are able to discriminate the sex of the emitter and that the behavioural response is sex-oriented, with male– male and female–female vocal interactions being the rule. In both species, these acoustic exchanges can be then described as an intra-sex communication system. Our experiments were performed during the

131

incubation period. At this stage, birds are paired and switch with their mate every few days to brood their egg in the burrow. The vocal behaviour observed is thus likely to be a sex-oriented territorial reaction: birds feel challenged by an intruder and discourage him by calling back, preventing usurpation of the burrow by a bird of its own sex. This reaction may also be a kind of mate guarding behaviour: the female or the male preventing another bird of the same sex to come into the nuptial burrow. A similar vocal response to calls of the same sex has been observed in the Manx shearwater (Brooke, 1978), the Greater shearwater (Brooke, 1988), and in other petrels such as the Thin-billed prion (Pachyptila belcheri; Bretagnolle, Genevois & Mougeot, 1998), the Leach’s storm-petrel (Taoka et al., 1989a), or the Swinhoe’s storm-petrel (Taoka, Won & Okumura, 1989b). Taken together, these findings suggest a strong level of intrasexual competition in burrowing petrels. However, the role of vocal sex recognition may vary according to the breeding stage (Storey, 1984; Bretagnolle et al., 1998). Thus, the incubation period is probably not favourable for courtship interactions with outsiders and this might explain the lack of reactivity of birds to the calls of the opposite sex.

INDIVIDUAL

VOCAL SIGNATURE: A DIVERGENCE IN

CALL STRUCTURE AND FUNCTION BETWEEN YELKOUAN AND CORY’S SHEARWATERS

According to our analysis, we found that individual identity information is encoded by acoustic cues in both species and both sexes. However, multivariate and univariate approaches underline that the call signature is more reliable in CS than in YS. In both species, the most individualized cues were related to the duration of call parts. The individual signature is thus mainly supported by temporal features as it has been reported for some other petrel species (Bretagnolle, 1996). However, the results of the present study show that frequency and energy features can also be important, making the individual signature a multi-parametric feature of the call. Indeed, fundamental frequency values of CS, and energy spectrum features of both sexes YS and female CS, were especially relevant in the vocal individual signature. PIC calculations generated greater values in CS than in YS, showing a higher potentiality for individual coding in the former species. Moreover, in CS, calls of a given individual were more stereotyped and showed a higher level of correct classification than in YS. Species whose birds breed close to each others are more likely to use well individualized vocal signatures to avoid confusion. This hypothesis cannot explain our results because YS nest closer from each other than CS (Bourgeois & Vidal, 2007).

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

132

C. CURE ET AL.

Playback experiments show a striking difference between the two species: whereas all tested CS responded to the voice of their mate but not to another opposite-sex bird, a majority of YS remained silent when hearing their mate or other opposite-sex birds. Thus, for CS, vocal exchanges appear to be the primary way to ensure mate recognition during the relay of incubation. Mates identify each other apparently with great accuracy, never confusing the mate with a stranger. This is probably linked to a well individualized vocal signature, as revealed by our acoustic analysis. Thus, CS reply to calls of the same sex in a territorial context, and to calls of the mate in a pair bonding context. Conversely, a great majority of tested YS did not reply to their mate’s call. This is true for both sexes, but females showed a tendency to be more reactive to their mate than males; indeed, in the rare cases where a response to the opposite sex was observed in females, it was always to the mate calls. The low level of vocal responses to the mate call observed in this species can be due to the fact that possibilities of confusion exist. Indeed, according to our analysis, the vocal signature of the YS is less individualized than in the CS and, consequently, birds of this species show more difficulties to identify the caller. It is also possible that YS need stimuli other than acoustics to identify an individual at the entrance of the burrow. Olfaction is well developed in petrel species (Bang, 1966; Bang & Wenzel, 1985; Bonadonna & Bretagnolle, 2002) and could be involved in mate recognition, as it has been experimentally demonstrated in the Antarctic prion (Pachyptila desolata; Bonadonna & Nevitt, 2004). Nevertheless, it has been shown that numerous species of petrels recognize the odour of their own burrow, suggesting that birds do not necessarily need to identify the mate (Bonadonna & Bretagnolle, 2002; Bonadonna et al., 2003, 2004). Tactile cues could be also a source of motivation, stimulating birds of the pair to call in duet once reunited within the burrow. Indeed, in natural condition, vocal duets in this species always begin once partners are reunited inside the burrow. At last, the quasi-absence of vocal response to mate calls in YS does not necessary mean that these birds are unable to recognize the call of their mate. A possibility would be that they seldom vocally reply to the mate during the incubation period. It has also been experimentally shown that two petrel species (the White-chinned petrel Procellaria aequinoctialis and the Grey petrel Procellaria cinerea; Brooke, 1986) vocally reply to the calls of strangers but remain silent to the playback of the mate call. YS could follow the same pattern of response. Moreover, petrels and particularly species of small size are subject to predation pressure (Imber, 1978; Martin, Thibault & Bretagnolle, 2000). A valuable anti-predator strategy would be to minimize the

emission of locatable acoustic signals (Mougeot & Bretagnolle, 2000), even if they are useful to communicate at night. Shearwaters and especially those of the smallest species, such as the YS, are preyed on by introduced mammals (Bonnaud et al., 2007). The greater risk of predation for the YS could explain why this species has possibly developed other alternative communication strategies than acoustic ones. To conclude, both CS and YS use a single call for mate recognition, mate attraction and nest defence. In both species, individuals react to vocal signals only if the identity signature (sexual or individual) of the emitter is well established. These two sympatric species seem to share a common maxim which could be summarized as ‘talk only if you know who is calling’. As for a majority of petrels, calls are sexually dimorphic and individuals do perceive sexual differences in voice. In both species, sex and individual vocal signatures appear to be multi-parametric. This coding strategy based on different parameters appears to be a mean to secure information transfer from the emitter to the receiver in the noisy environment of a seabird colony (Aubin & Jouventin, 2002). Nevertheless, in spite of similar environmental constraints, these two sympatric and related shearwater species differ in regard to mate identification. Whereas CS can rely on an accurate individual vocal signature to recognize their mate, a less reliable signature in YS call may be correlated to the need of cues other than acoustic ones for mate identification. Thus, if some breeding strategies (such as burrow defence behaviour) appear to be similar among many shearwaters and even many petrels, others (such as pair bond maintenance) can vary according to the species, even in a sympatric context.

ACKNOWLEDGEMENTS This study was supported by the CNRS and the UE Life project (contract ref. LIFE03NAT/F000105). C.C. is funded by a Big Mat grant and N.M. is funded by the Institut Universitaire de France. We are very grateful to the staff of Port-Cros National Park and Porquerolles Island, especially to J. B. Milcamps, H. Bergère, and S. Dromzé, who allowed us to conduct this research. We are also grateful to E. Vidal, K. Bourgeois, J. Legrand (IMEP-CNRS of Aix en Provence), and M. Lascève (LPO PACA), who all contributed to over the course of the field work. We are also grateful to Joël White for comments and improvement of the English.

REFERENCES Aubin T. 1994. Syntana: a software for the synthesis and analysis of animal sounds. Bioacoustics 6: 80–81.

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

ACOUSTIC COMMUNICATION IN TWO SYMPATRIC SHEARWATERS Aubin T, Jouventin P. 1998. Cocktail party effect in king penguin colonies. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 1665–1673. Aubin T, Jouventin P. 2002. How to identify vocally a kin in a crowd? The penguin model. Advances in the Study of Behaviour 31: 243–277. Bang BG. 1966. The olfactory apparatus of tubenosed birds (Procellariiformes). Acta Anatomica 65: 391–415. Bang BG, Wenzel BM. 1985. Nasal cavity and olfactory system. In: King AS, McLelland J, eds. Form and function in birds. London: Academic Press, 195–225. Bonadonna F, Bretagnolle V. 2002. Smelling home: a good solution for burrow-finding in nocturnal petrels? Journal of Experimental Biology 205: 2519–2523. Bonadonna F, Cunningham GB, Jouventin P, Hesters F, Nevitt GA. 2003. Evidence for nest-odour recognition in two species of diving petrel. Journal of Experimental Biology 206: 3719–3722. Bonadonna F, Nevitt GA. 2004. Partner-specific odor recognition in an Antarctic seabird. Science 306: 835. Bonadonna F, Villafane M, Bajzak C, Jouventin P. 2004. Recognition of burrow’s olfactory signature in blue petrels, Halobaena caerulea: an efficient discrimination mechanism in the dark. Animal Behaviour 67: 893–898. Bonnaud E, Bourgeois K, Vidal E, Kayser Y, Tranchant Y, Legrand J. 2007. Feeding ecology of feral cat population on a small Mediterranean Island. Journal of Mammalogy 88: 1074–1081. Bourgeois K. 2006. Ecologie et Conservation d’un oiseau marin endémique de Méditerranée Puffinus yelkouan. PhD Thesis, University of Aix-Marseille III. Bourgeois K, Curé C, Legrand J, Gómez-Díaz E, Vidal E, Aubin T, Mathevon N. 2007. Morphological versus acoustic analysis: what is the most efficient method for sexing Yelkouan shearwaters Puffinus yelkouan? Journal of Ornithology 148: 261–269. Bourgeois K, Vidal E. 2007. Yelkouan shearwater nestcavity selection and breeding success. Comptes Rendus Biologies 330: 205–214. Bradley JS, Woller RD, Skira IJ, Serventy DL. 1990. The influence of mate retention and divorce upon reproductive success in Short-tailed shearwaters Puffinus tenuirostris. Journal of Animal Ecology 59: 487–496. Bretagnolle V. 1996. Acoustic communication in a group of non-passerine birds, the petrels. In: Kroodsma DE, Miller EH, eds. Ecology and evolution of acoustic communication in birds. Ithaca, NY: Cornel University Press, 160– 178. Bretagnolle V, Genevois F, Mougeot F. 1998. Intra- and intersexual functions in the call of a non-passerine bird. Behaviour 135: 1161–1184. Bretagnolle V, Lequette B. 1990. Structural variation in the call of the Cory’s shearwater (Calonectris diomedea, Aves, Procellariidae). Ethology 85: 313–323. Bretagnolle V, Thibault JC. 1995. Method for sexing fledgings in Cory’s shearwaters and comments on sex-ratio variation. Auk 112: 785–790. Bried J, Pontier D, Jouventin P. 2003. Mate fidelity in

133

monogamous birds: a re-examination of the Procellariiformes. Animal Behaviour 65: 235–246. Brooke MDL. 1978. Sexual differences in the voice and individual vocal recognition in the Manx shearwater (Puffinus puffinus). Animal Behaviour 26: 622–629. Brooke MDL. 1986. The vocal systems of two nocturnal burrowing petrels, the White-chinned Procellaria aequinoctialis and the Grey P. cinerea. The Ibis 128: 502–512. Brooke MDL. 1988. Sexual dimorphism in the voice of the Greater shearwater. Wilson Bulletin 100: 319–323. Brooke MDL. 1990. The Manx shearwater. London: Academic Press. Brooke MDL, Prince PA. 1990. Nocturnality in seabirds. Acta XX Congressus Internationalis Ornithologici II: 1113– 1121. Charrier I, Mathevon N, Jouventin P, Aubin T. 2001. Acoustic communication in a black-headed gull colony: how chicks identify their parents? Ethology 107: 964–974. Del Hoyo J, Elliott A, Sargatal J. 1992. Handbook of the birds of the world: ostrich to ducks. Barcelona: Lynx Edicions. Falls JB. 1982. Individual recognition by sounds in birds. In: Kroodsma DE, Miller EH, eds. Acoustic communication in birds, Vol. 2. New York, NY: Academic Press, 237–278. Fletcher NH. 2004. A simple frequency-scaling rule for animal communication. Journal of the Acoustical Society of America 114: 2334–2338. Imber MJ. 1978. The effects of rats on breeding success of petrels. In: Dingwall PR, Atkinson IAE, Hay C, eds. The ecology and control of rodents in New Zealand Nature Reserves. Auckland: Department of Land and Survey Information Series, 67–71. James PC, Robertson HA. 1985a. Sexual dimorphism in the voice of the Little shearwater Puffinus assimilis. The Ibis 127: 388–390. James PC, Robertson HA. 1985b. The call of Bulwer’s petrel (Bulweria bulwerii), and the relationship between intersexual call divergence and aerial calling in the nocturnal Procellariiformes. Auk 102: 878–881. Jouventin P, Aubin T. 2002. Acoustic systems are adapted to breeding ecologies: individual recognition in nesting penguins. Animal Behaviour 64: 747–757. Keppel G. 1991. Design and analysis, a researcher’s handbook. Englewood Cliffs, NJ: Prentice-Hall Inc. Lachenbruch PA, Mickey MR. 1968. Estimation of error rates in discriminant analysis. Technometrics 10: 1–11. Lengagne T, Jouventin P, Aubin T. 1999. Finding one’s mate in a king penguin colony: efficiency of acoustic communication. Behaviour 136: 833–846. Lind H, Dabelsteen T, McGregor PK. 1996. Female Great Tits can identify mates by song. Animal Behaviour 52: 667–671. Lo Valvo M. 2001. Sexing adult Cory’s shearwater by discriminant analysis of body measurements on Linosa Island (Sicilian Channel), Italy. Waterbirds 24: 169–174. McGregor PK, Catchpole CK, Dabelsteen T, Falls JB, Fusani L, Gerhardt HC, Gilbert F, Horn AG, Klump GM, Kroodsma DE, Lambrechts MM, McComb KE,

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134

134

C. CURE ET AL.

Nelson DA, Pepperberg IM, Ratcliffe L, Searcy WA, Weary DM. 1992. Design of playback experiments: the Thornbridge Hall NATO ARW consensus. In: McGegor PK, ed. Playback and studies of animal communication. New York, NY: Plenum Press. Mackin WA. 2005. Neighbour-stranger discrimination in Audubon’s shearwater (Puffinus l. lherminieri) explained by a ‘real enemy’ effect. Behavioral Ecology and Sociobioly 59: 326–332. McNeil R, Drapeau P, Pierrotti R. 1993. Nocturnality in colonial waterbirds: occurrence, special adaptations and suspected benefits. In: Power DM, ed. Current ornithology. New York, NY: Plenum Press, 187–246. Martin JL, Thibault JC, Bretagnolle V. 2000. Black rats, island characteristics and colonial birds in the Mediterranean: consequences of an ancient introduction. Conservation Biology 14: 1452–1466. Mathevon N, Aubin T, Vielliard J, Da Silva ML, Sebe F, Boscolo D. 2008. Singing in the rainforest: how a tropical bird song transfers information. PloS ONE 3: e1580. Mathevon N, Charrier I, Jouventin P. 2003. Potential for individual recognition in acoustic signals: a comparative study of two gulls with different nesting patterns. Comptes Rendus Biologies 326: 329–337. Miller DB. 1979. The acoustic basis of mate recognition by female zebra finches, Taeniopygia guttata. Animal Behaviour 27: 376–380. Mougeot F, Bretagnolle V. 2000. Predation as a cost of sexual communication in nocturnal seabirds: an experimental approach using acoustic signals. Animal Behaviour 60: 647–656. Mougin JL. 2000. Pairing in the Cory’s shearwater (Calonectris diomedea) of Selvagem Grande. Journal für Ornithologie 141: 319–326. Mougin JL, Granadeiro JP, Jouanin C, Roux F. 1999. Philopatry and faithfulness to nest site in Cory’s shearwaters Calonectris diomedea at Selvagem Grande. Ostrich 70: 229–232. O’Loghlen AL, Beecher MD. 1997. Sexual preferences for mate song types in female song sparrows. Animal Behaviour 53: 835–841. R Development Core Team. 2007. R: a language and environment for statistical computing, Version 2.5.0. Vienna: R Foundation for Statistical Computing. Randall RB, Tech BA. 1987. Frequency analysis. Naerum: Bruël & Kjaer Press. Ristow D, Wink M. 1980. Sexual dimorphism of Cory’s shearwater. Il-Merill 21: 9–12. Robinson P, Aubin T, Brémond J. 1993. Individuality in the voice of emperor penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology 94: 279–290. Scherrer B. 1984. Bioacoustique. Quebec: Gaëtan-Morin Press.

Slabbekoorn H. 2004. Singing in the wild: the ecology of birdsong. In: Marler P, Slabbekoorn H, eds. Nature’s music: the science of birdsong. San Diego, CA: Academic Press, 178–205. Specht R. 2004. Avisoft-SAS Lab Pro, Version 4.39. Berlin: Avisoft Bioacoustics. StatSoft. 2001. Statistica, Version 6.0 for windows (computer manual). Tulsa, OK: Statsoft Inc. Storey AE. 1984. Function of the Manx shearwater calls in mate attraction. Behaviour 89: 73–89. Taoka M, Okumura H. 1990. Sexual differences in flight calls and the cue for vocal sex recognition of Swinshoe’s storm-petrels. Condor 92: 571–575. Taoka M, Sato T, Kamada T, Okumura H. 1989a. Sexual dimorphism of chatter-calls and vocal sex recognition in Leach’s storm-petrels (Oceanodroma leucorhoa). Auk 106: 498–500. Taoka M, Won P, Okumura H. 1989b. Vocal behavior of Swinhoe’s storm-petrel (Oceanodroma monorhis). Auk 106: 471–474. Thibault JC. 1985. La reproduction du puffin cendré Calonectris diomedea en Corse. In: Marins Nicheurs du Midi et de la Corse. Aix-en-Provence: Annales de Centre de Recherches Ornithologiques de Provence, 49–55. Thibault JC. 1994. Nest-site tenacity and mate fidelity in relation to breeding success in Cory’s shearwater Calonectris diomedea. Bird Study 41: 25–28. Tibbetts EA, Dale J. 2007. Individual recognition: it is good to be different. Trends in Ecology and Evolution 22: 529– 537. Venables WN, Ripley BD. 2002. Modern applied statistics with S. New York, NY: Springer. Vidal P. 1985. Premières observations sur la biologie de reproduction du puffin des Anglais yelkouan Puffinus puffinus yelkouan sur les îles d’Hyères (France). In: Oiseaux marins nicheurs du Midi et de la Corse. Aix-en-Provence: Annales du Centre de Recherches Ornithologiques de Provence, 58–62. Wallschläger D. 1980. Correlate of song frequency and body weight in passerine birds. Experientia 36: 412. Warham J. 1990. The Petrels: their ecology and breeding systems. London: Academic Press. Warham J. 1996. The behaviour, population biology and physiology of the petrels. London: Academic Press. Wiley RH, Richards DG. 1982. Adaptations for acoustic communication in birds: transmission and signal detection. In: Kroodsma DE, Miller EH, eds. Acoustic communication in birds, Vol. 2. New York, NY: Academic Press, 131– 181. Wink M, Wink C, Ristow D. 1982. Brutbiologie mediterraner Gelbschnabelsturmtaucher Calonectris diomedea diomedea. Seevögel Suppl: 127–135.

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 115–134