Variation in Guiana dolphin (Sotalia guianensis) whistles: using a broadband recording system...

acta ethol DOI 10.1007/s10211-014-0183-7

ORIGINAL PAPER

Variation in Guiana dolphin (Sotalia guianensis) whistles: using a broadband recording system to analyze acoustic parameters in three areas of southeastern Brazil Luciana Guimarães de Andrade & Isabela Maria Seabra Lima & Halerson da Silva Macedo & Rafael Ramos de Carvalho & José Lailson-Brito Jr. & Leonardo Flach & Alexandre de Freitas Azevedo

Received: 21 June 2013 / Revised: 9 October 2013 / Accepted: 13 February 2014 # Springer-Verlag Berlin Heidelberg and ISPA 2014

Abstract The Guiana dolphin produces a variable whistle repertoire related to different social contexts. The current study evaluates Guiana dolphin whistles at a microscale.

Acoustic parameters of whistles were compared between three areas in southeastern Brazil using a recording system with sampling rate of 96 kHz. Previous studies that utilized a sampling rate of 48 kHz reported little variation between adjacent areas in Brazil. Nine acoustic parameters of the whistles (duration, start, end, minimum and maximum frequencies, delta frequency, frequency at 1/4, 1/2, and 3/4 of duration) were measured and whistles were classified into five contour forms. A total of 659 whistles were analyzed, of which 62.20 % showed an ascending contour form. The Guiana dolphin emitted whistles with a fundamental frequency reaching 44.9 kHz. Dolphin whistles from the three study areas varied significantly in nine acoustic parameters. The whistle duration was shorter (272.44 ± 105.25 ms) in Guanabara Bay than those in Sepetiba (360.05±135.16 ms) and Paraty Bays (376.80±159.78 ms). The start and minimum frequencies of the whistles in Guanabara Bay was significantly higher than those in Sepetiba and Paraty Bays. The results L. G. de Andrade : J. Lailson-Brito Jr. : A. de Freitas Azevedo Pós-Graduação em Ecologia e Evolução (PPGEE), Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, Maracanã, Rio de Janeiro 20550-013, Rio de Janeiro, Brazil L. G. de Andrade (*) : I. M. Lima : H. da Silva Macedo : R. R. de Carvalho : J. Lailson-Brito Jr. : A. de Freitas Azevedo Faculdade de Oceanografia (FAOC), Laboratório de Mamíferos Aquáticos e Bioindicadores (MAQUA), Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier 524, Maracanã, Rio de Janeiro 20550-013, Rio de Janeiro, Brazil e-mail: andrade.uerj@gmail.com L. Flach Instituto Boto Cinza, Rua Santa Terezinha 531, Rio de Janeiro 23860-000, Rio de Janeiro, Brazil

of discriminant function analysis indicated a significant difference between Guanabara Bay and the other two areas.

Comparisons of the ascending, descending–ascending, and multi whistles between areas showed differences in some acoustic parameters. In this study, by doubling the sampling rate in our recording systems, we were able to more accurately sample the whistle repertoire of Guiana dolphins in southeastern Brazil, and thereby detect differences in whistles between neighboring populations.

Keywords Sotalia guianensis . Whistles . Microscale variation . Bioacoustic

Introduction Delphinids produce a variety of acoustic emissions used in different behavioral contexts, including recruitment during feeding activities and group cohesion (Caldwell et al. 1990; Richardson et al. 1995; Tyack 2000; Podos et al. 2002).

Dolphin acoustic signals are divided into two broad categories: whistles (tonal sounds) and pulsed sounds (Richardson et al.

1995). Whistles are continuous, narrow-band sounds that often exhibit frequency modulation and harmonics (Richardson et al.

1995; Tyack 2000). Fundamental frequencies of whistles are typically between 800 and 28.5 kHz, with durations between 100 ms and 4 s (Schultz and Corkeron 1994; Buckstaff 2004; Janik 2009). This type of sound emission is used mainly in social contexts such as group coordination, behavioral activities, and individual identification (e.g., Caldwell et al. 1990; Janik et al. 1994; Herzing 2000; Van Parijs and Corkeron 2001; Pivari and Rosso 2005; Janik 2009; Díaz López 2011).

Several studies have used qualitative analyses (related to variations in the contour form) and quantitative analyses (duration and frequency measurements) of whistles to characterize

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populations and species of delphinids (e.g., Steiner 1981; Rendell et al. 1999; Bazúa-Durán and Au 2002; Oswald et al. 2004).

Comparative studies indicate that whistles show variation in acoustic parameters between species and populations (Wang et al. 1995a; Bazúa-Durán and Au 2004; Azevedo and Van Sluys 2005; Rossi-Santos and Podos 2006; Ansmann et al.

2007). This variability may be related to factors such as adaptation to differences in behavior, body size, learning stage, and adaptation to different environments (Wang et al. 1995a; Mathews et al.

1999; Morisaka et al. 2005; Rossi-Santos and Podos 2006; May-Collado et al. 2007). Comparisons of whistles may reveal the distinct characteristics of each population, including different aspects of ecology. They also allow the identification at the species and, in some cases, population level that require conservation and management actions (Wang et al. 1995a; Wang et al.

1995b, Morisaka et al. 2005, May-Collado and Wartzok 2008).

Additionally, intraspecific comparisons of whistle parameters among groups facing different environmental conditions may provide information about the influence of habitat on the characteristics of this type of acoustic emission (Wang et al. 1995b).

The Guiana dolphin (Sotalia guianensis) has a varied whistle repertoire related to behavioral activities and social interactions.

Most acoustic studies of this species in Brazil have focused on whistles (Monteiro Filho and Monteiro 2001; Azevedo and Simão 2002; Erber and Simão 2004; Pivari and Rosso 2005; Azevedo and Van Sluys 2005; Rossi-Santos and Podos 2006).

Some studies in Brazil have shown that Guiana dolphin whistles vary intraspecifically, with major variation in nonadjacent populations (Azevedo and Van Sluys 2005; RossiSantos and Podos 2006). In Brazil, Azevedo and Van Sluys (2005) used a recording system with a 48 kHz sampling rate, which, as per the Nyquist sampling theorem, has limited the maximum recordable whistle frequency to 24 kHz (Au and Hastings 2008). These authors reported the broadest whistle frequency range from 1.34 to 23.89 kHz, and they noted whistles cut off by the upper frequency limit of the recording system beyond 24 kHz. The same authors suggested the use of a broadband recording system to analyze whistle structures.

Bandwidth limit has been shown to have an important effect on the correct classification of whistles among dolphin species (Oswald et al. 2004; May-Collado and Wartzok 2009). A recent study in Costa Rica has shown that Guiana dolphins can emit whistles with frequencies up to 48.4 kHz (MayCollado and Wartzok 2009). This suggests that comparisons in dolphin whistle acoustic structure between areas in Brazil have been made while only considering a fraction of the actual whistle repertoire of the species. The goal of this study is to investigate the variation in the whistles of Guiana dolphin from different geographical locations in southeastern Brazil.

This study provides new information about Guiana dolphin whistle characteristics using a recording system with a 96-kHz sampling rate and compares acoustic parameters of Guiana dolphin whistles among three adjacent populations.

Materials and methods Study areas and data collection Surveys and recordings of Guiana dolphin emissions were performed at three coastal bays (Guanabara, Sepetiba, and Paraty Bays), Rio de Janeiro State, southeastern Brazil, between July 2008 and July 2009 (Fig. 1). Each of these bays hosts a resident population of Guiana dolphin (Lodi 2003; Azevedo et al. 2004; Azevedo et al. 2005; Azevedo et al. 2007; Flach et al. 2008). Other delphinid species can occasionally be found mainly near the entrance of the bays, but only Guiana dolphins were recorded in this study. The recordings in Guanabara Bay (22°50′S, 43°10′ W) were made over 9 months, in Sepetiba Bay (22°54′S, 44°10′W) over 3 months, and in Paraty Bay (22°54′S, 44°10′W) over 6 months. All recordings were carried out under similar weather conditions (Beaufort Sea states ≤2) in small (4.5–6.6 m long) outboard-powered boats.

Acoustic recordings were made with the engine turned off and were monitored with headphones. The recording system consisted of one C54XRS hydrophone with a frequency response from 0.009 to 100 kHz (+3/−12 dB, −165 dB re: 1 V/μPa) (Cetacean Research Technology, WA, USA) and a Marantz PMD 671 digital recorder with a sampling rate of 96 kHz and a bit depth of 24 bits. The boat was positioned approximately 30 m from the sampled group to avoid possible interference with behavior. The hydrophone was positioned at a depth of 2 m, and recordings were made for each group or behavioral activity.

For each group of S. guianensis observed, the GPS location, time, group size, group composition, and behavior were recorded. The recordings were made during three behavioral activities: traveling, foraging and/or feeding, and socializing (Table 1). Groups were defined as two or more dolphins in which each individual was within 10 m of at least one other member of the group (Quick and Janik 2008).

Analysis of whistles Analyses were limited to whistles with the start and end frequency clearly visible and an absence of overlapping whistles. A sample of whistles was randomly selected from different recording days, different groups, and different behavioral activities in each study to minimize the sampling problem with independence of data. The maximum number of whistles analyzed for each group was up to twice the number of individuals in the group (see Azevedo and Van Sluys 2005).

Approximately 27 h of acoustic recordings were analyzed.

During the recordings, the group size of Guiana dolphins varied between 8 and 150 individuals.

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Fig. 1 Map showing the three bays and the local surveys (black points) on the Rio de Janeiro coast, southeastern Brazil, where Guiana dolphin whistles were recorded

The program used for the analysis of the whistles was RAVEN 1.1 (Cornell Laboratory of Ornithology, NY, USA).

The analysis included a fast Fourier transform (FFT) size of 512 points, an overlap of 50 %, and a Hanning window. Two methods were applied for the comparative analysis of whistles: (i) a qualitative analysis of whistles classified into five contour form categories and (ii) a quantitative analysis involving the determination of frequency and duration measures for each whistle.

The contour of each whistle and the classification into five contour form categories (ascending, ascending–descending, descending–ascending, constant, and multi) were determined through visual analyses of the frequency modulation by at

least two of the authors (see Azevedo and Van Sluys 2005) (Fig. 2). Multi whistle was defined as whistle with more than one inflection point.

Nine acoustic variables were measured on the fundamental component frequency of whistles: starting frequency (SF), ending frequency (EF), minimum frequency (Mn.F), maximum frequency (Mx.F), delta frequency (DF) (Mx.F−Mn.F), duration (D), frequency at 1/4 of duration (F¼), frequency at 1/2 of duration (F½), and frequency at 3/4 of duration (F¾). The number of inflection points (points at which the form of the whistle contour changes from ascending to descending and vice versa), breaking contour points (Bc) (points where

Table 1 Group size with the mean, standard deviation, minimum and maximum values, group composition, behavior (foraging, traveling, and socializing), recording days, and recording time for whistles of the

Guiana dolphin in Guanabara Bay (N=203), Sepetiba Bay (N=234), and Paraty Bay (N=222)

Locality

Group size (min–max) mean±SD

Group composition

Behavior

Recording days

Recording time

Guanabara Bay Sepetiba Bay Paraty Bay

8–24 12.6±6.4 20–150 86.6±35.0 20–120 64.8±34.2

Adults, juveniles, and calves Adults, juveniles, and calves Adults, juveniles, and calves

Foraging, traveling, and socializing Foraging, traveling, and socializing Foraging, traveling, and socializing

19 6 9

13 h 3 min 5 h 28 min 7 h 23 min

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Fig. 2 Contour form categories of Guiana dolphin whistles. Ascending (a), ascending–descending (b), descending–ascending (c), multi (d), and constant (e)

the whistle has a break in contour form without a change in form) and harmonics was quantified. The frequency

variables were measured in kilohertz (kHz) and the duration in milliseconds (ms).

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Statistical analysis A chi-squared test (P<0.01) was used to investigate the relative frequency of occurrence of the five contour forms.

Descriptive statistics, including minimum and maximum values, mean, standard deviation, and median, were used to characterize all acoustic parameters. The Levene test (P<0.05) was applied to test the variance of the data. The acoustic parameters of the whistles from the three areas were compared using two methods. First, the Kruskal-Wallis test (P<0.025) was used, and after the variables were rankordered, the post hoc Tukey test (P<0.05) was applied to identify the variables that differ between areas (Zar 1999).

The same tests were applied to compare whistles with the same contour between areas. The testing of many different variables on the same whistles can create a data dependence problem. In order to minimize this problem, the Bonferroni procedure was applied to adjust the level of significance to the Kruskal-Wallis test.

Second, the frequency parameters, duration, and inflection point were used in a discriminant function analysis (DFA) to investigate variations in acoustic parameters of whistles between areas throughout a linear combination of quantitative predictor variables that best characterize the differences between groups.

Results A total of 659 whistles were analyzed: 203 from Guanabara Bay, 234 from Sepetiba Bay, and 222 from Paraty Bay. Ascending whistles were the most frequent in all three areas and corresponded to 62.2 % of all whistles (N=446). Multi whistles were the second most frequent, corresponding to 17.29 % of all whistles (N=124). However, the use of the five contour form categories varied between areas (Χ2 =29.40, df=4) (Table 2).

Descriptive statistics of acoustic variables of whistles are shown in Table 3. Differences between the three areas were found in nine acoustic variables (Kruskal-Wallis test, H (2, N=659); P<0.025): D, SF, EF, Mn.F, Mx.F, DF, F¼, F½, F¾ and Bc. The whistle duration was shorter (272.44±105.25 ms) Table 2 Number of whistles in each of five contour categories in three study areas

in Guanabara Bay than those in Sepetiba (360.05±135.16 ms) and Paraty Bays (376.80±159.78 ms) (Tukey post hoc test, df=656, P<0.05; Table 4).

The Guiana dolphin emitted whistles with a fundamental frequency reaching 44.9 kHz. Whistles with an end frequency beyond 24 kHz (the frequency limit of the recording system used in other studies with this species in Brazil) represented 37 % (N=244) of all whistles analyzed. The whistle frequency values ranged from 2.15 to 42.65 kHz in Guanabara Bay, from 1.87 to 44.9 kHz in Sepetiba Bay, and from 1.03 to 42.84 kHz in Paraty Bay. Within this frequency range, EF, Mx.F, F¼, F½, and F¾ were significantly different between the three study areas, with higher mean values found in Guanabara Bay (Table 4).

The SF of the whistles (9.88±3.90 kHz) from Guanabara Bay was significantly higher than those from Sepetiba (7.93±2.47 kHz) and Paraty Bays (8.09±2.49 kHz) (Tukey post hoc test, df=656, P<0.05; Table 4). A similar pattern was found for Mn.F with values in Guanabara Bay (9.52 ± 3.55 kHz) greater than those from Sepetiba (7.87±2.32 kHz) or Paraty Bay (7.74±2.20 kHz) (Tukey post hoc test, df=656, P<0.05; Table 4).

Significant differences between Guanabara and Sepetiba Bays were found for eight acoustic parameters (D, SF, EF, Mn.F, Mx.F, F¼, F½, F¾), and differences between Guanabara and Paraty Bays were found for nine acoustic parameters (SF, EF, Mn.F, Mx.F, DF, D, F¼, F½, and F¾) and breaking contour. Differences were found in four acoustic parameters (DF, F¼, F½, and F¾) between Sepetiba and Paraty Bays (Table 4; Tukey post hoc test; P<0.05). The results of discriminant function analysis indicated a significant difference between Guanabara Bay and the other two areas (Wilks’ lambda=0.75698; F (12.1418)=17.650 P<0.0001).

Five whistle variables contributed to discriminant function (SF, EF, D, F¼, and F¾); however, the duration of whistles was the main acoustic parameter that contributed to the difference between areas. Whistles were more similar between Sepetiba and Paraty Bays (D2 =0.504673, F values=10.53) than in Guanabara Bay (Fig. 3). The Mahalanobis distance (D2) value was higher between Guanabara and Paraty Bays than that between Guanabara (D2 =1.617607, F values= 28.38) and Sepetiba Bays (D2 =0.08739, F values=17.05) (Fig. 3).

Whistle contour category Study area

Ascending (N=409)

Ascending–descending (N=28)

Descending–ascending (N=101)

Constant (N=9)

Multi (N=112)

Guanabara Bay Sepetiba Bay Paraty Bay

128 137 144

4 20 4

30 30 41

0 3 6

41 44 27

acta ethol Table 3 Descriptive statistics (mean, standard deviation, median, minimum, and maximum values) for nine acoustic parameters, inflection points, and breaking contours of Guiana dolphin whistles in Guanabara, Sepetiba, and Paraty Bays, southeastern Brazil. The duration was measured in ms and the frequency parameters in kHz.

Acoustic parameters

Guanabara Bay (N=203)

Sepetiba Bay (N=234)

Paraty Bay (N=222)

Duration

272.44±105.25 267.00 100–652 9.88±3.90 9.00

360.05±135.16 357.50 111–826 7.93±2.47 7.91

376.80±159.78 370.50 104–1231 8.09±2.49 7.87

2.15–26.53 25.58±7.38 26.62 8.90–42.65 9.52±3.55 8.81 2.15–25.40 25.79±7.51 26.90 8.90–42.65 16.52±7.81 16.39 0.84–34.78 12.79±3.74 12.84 5.72–30.37 16.54±4.80 16.12

1.87–16.40 23.42±7.78 21.93 4.31–44.90 7.77±2.32 7.73 1.87–15.46 23.68±7.76 22.59 4.31–44.90 15.91±7.87 14.45 0.47–41.71 11.32±3.80 10.49 2.43–28.59 15.02±5.21 14.71

1.03–17.71 22.26±7.99 21.00 4.59–42.84 7.74±2.20 7.68 1.03–14.53 22.33±7.94 21.00 4.59–42.84 14.56±8.30 12.41 0.65–35.52 10.29±2.94 9.93 3.65–20.15 13.00±4.34 12.00

7.03–30.93 20.96±6.07 20.53 7.78–35.34 0.66±1.07 0 0–7 1.05±1.48 1 0–10

3.09–34.78 19.27±5.20 19.78 4.21–40.78 0.60±0.88 0 0–4 0.83±1.20 0 0–7

4.21–28.68 16.72±6.07 16.12 4.22–33.00 0.45±0.74 0 0–3 0.59±0.84 0

SF

EF

Mn.F

Mx.F

DF

F¼

F½

F¾

Inflection point

Bc

Comparisons between contour form categories Ascending, descending–ascending, and multi whistles were compared between areas. Only these three categories were selected for comparison due to the sample size (Table 2).

Ascending whistles showed significant differences in D, EF, Mx.F, F¼, F½, and F¾ (Kruskal-Wallis test, H (2, N=446); P<0.025). Two acoustic parameters of the ascending whistles (D and F¼) differed significantly between Guanabara and Sepetiba Bays (Tukey post hoc test, P<0.05; Table 4). Significant differences were found between Guanabara and Paraty Bays for six acoustic parameters (D, EF, Mx.F, F¼, F½, and F¾ (Tukey post hoc test, P<0.05; Table 4). Four acoustic

0–4

parameters (EF, Mx.F, F½, and F¾) differed significantly between Sepetiba and Paraty Bays (Tukey post hoc test, P<0.05; Table 4).

The comparison of the acoustic parameters of descending– ascending whistles showed significant differences between Guanabara Bay and the two other areas for SF, EF, Mn.F, Mx.F, F¼, F½, and F¾ (Tukey post hoc test, P <0.05; Table 4). No differences were found in acoustic parameters of descending–ascending whistles between Sepetiba and Paraty Bays.

For the multi whistles, six whistle variables differed significantly between Guanabara and the two other areas (D, SF, Mn.F, F¼, F½, and F¾), and two variables (F¼ and F½) were different between Paraty and Sepetiba Bays (Tukey post hoc test, P<0.05; Table 4).

acta ethol Table 4 Tukey post hoc test (P<0.05) results for comparisons of acoustic variables of all whistles, ascending, descending–ascending, and multi whistles of the Guiana dolphin in the three study areas Guanabara Bay (GB), Sepetiba Bay (SB), and Paraty Bay (PB) Acoustic variables

Total whistles (N=659)

Ascending whistles (N=409)

Descending–ascending whistles (N=101)

Multi whistles (N=112)

Inflection point Bc

NS GB×PB (P=0.002) GB×SB (P=0.000022) GB×PB (P=0.000022) GB×SB (P=0.000022) GB×PB (P=0.000036) GB×SB (P=0.018059) GB×PB (P=0.000028) GB×SB (P=0.000022) GB×PB (P=0.000022) GB×SB (P=0.029460) GB×PB (P=0.000025) GB×PB (P=0.031921) SB×PB (P=0.023091) GB×SB (P=0.000114) GB×PB (P=0.000022) SB×PB (P=0.001284) GB×SB (P=0.005268) GB×PB (P=0.000022) SB×PB (P=0.000022) GB×SB (P=0.028158) GB×PB (P=0.000022) SB×PB (P=0.000022)

– NS

– NS

NS NS

GB×SB (P=0.000022) GB×PB (P=0.000022) NS

NS

GB×SB (P=0.001348) GB×PB (P=0.007488) GB×SB (P=0.000022) GB×PB (P=0.000022) NS

Duration

SF

EF

Mn.F

Mx.F

DF

F¼

F½

F¾

GB×PB (P=0.041519) SB×PB (P=0.020911) NS

GB×SB (P=0.000741) GB×PB (P=0.021850) GB×SB (P=0.043207) GB×PB (P=0.003767) GB×SB (P=0.001386) GB×PB (P=0.003473) GB×SB (P=0.044203) GB×PB (P=0.003831) NS

GB×SB (P=0.024959) GB×PB (P=0.000682)

GB×SB (P=0.000125) GB×PB (P=0.000131)

GB×PB (P=0.000083) SB×PB (P=0.000526)

GB×PB (P=0.000031) SB×PB (P=0.004303)

GB×SB (P=0.001352) GB×PB (P=0.000109)

GB×PB (P=0.001709) SB×PB (P=0.023417)

GB×PB (P=0.000070) SB×PB (P=0.000036)

GB×SB (P=0.011015) GB×PB (P=0.000115)

GB×SB (P=0.016743)

GB×PB (P=0.047386) SB×PB (P=0.02062) NS

GB×SB (P=0.000022) GB×PB (P=0.000022) NS

NS

NS no significant difference

Discussion The frequency range values of the whistles reported in this study (1.03–44.9) were higher than the values from previous studies in Brazil (Monteiro Filho and Monteito 2001; Azevedo and Simão 2002; Erber and Simão 2004; Azevedo and Van Sluys 2005; Pivari and Rosso 2005; Rossi-Santos and Podos 2006). The upper frequency limits used in these

previous studies (18 and 24 kHz) might have limited the whistle repertoire and restricted the analyses of the variables (Table 5). A study in Sepetiba Bay reported Mx.F of Guiana dolphin whistles up to 17.49 kHz (Erber and Simão 2004) whereas our results showed Mx.F of whistles in the same area up to 44.90 kHz. The same pattern can be observed between previous studies in Guanabara Bay, with Mx.F of whistles up to 18 and 23.75 kHz (Azevedo and Simão 2002; Azevedo and

acta ethol Fig. 3 Means of the canonical variables (CV) for the betweengroup pairwise comparison of Guiana dolphin whistles among three areas (Guanabara, Sepetiba, and Paraty Bays)

van Sluys 2005, respectively), and our results with Mx.F of whistles up to 42.65 kHz. The broader frequency range of our recording system allowed for the more accurate analysis of whistle duration and maximum frequency, and it was important in determining differences in whistle structures between areas. According to Azevedo and Van Sluys (2005), the low degree of discrimination previously found between adjacent areas may have been related to the frequency limit of the recording systems. The authors identified 16 % of all selected whistles as being cut off by the upper frequency limit of their recording system (Azevedo and Van Sluys 2005). The limits of the recording systems used can restrict the selection of whistles for analysis, making it difficult to characterize the whistle repertoire of certain odontocete species (Bazúa-Durán 2004; Oswald et al. 2004).

Whistles emitted by Guiana dolphins varied between study areas. In Guanabara Bay, whistles were significantly different than whistles in Sepetiba and Paraty Bays. Eight acoustic parameters were different between Guanabara and Sepetiba Bays (70 km apart) whereas nine acoustic variables differed between Guanabara and Paraty Bays (120 km apart). Four acoustic variables were different between Sepetiba and Paraty Bays (50 km apart). These differences found in the whistles of Guiana dolphin agree with the possible movement of animals between areas. Movement of individuals between Sepetiba and Paraty Bays seems to be more frequent than movements between those two areas and Guanabara Bay (unpublished data), which might explain the lower variation in acoustic parameters of whistles between Sepetiba and Paraty Bays.

Rossi-Santos and Podos (2006) reported a discontinuity in whistle start and minimum frequencies between south and north areas in Brazil, and these authors suggested that this pattern could be associated with limited movement of animals

between areas. Several studies have investigated whistle variations relating to geographic distance with Guiana dolphin (e.g., Azevedo and Van Sluys 2005; Rossi-Santos and Podos 2006) and with other delphinid species (Wang et al. 1995a; Bazúa-Dúran and Au 2002; Bazúa-Dúran and Au 2004). Our findings showed that the start and minimum frequencies were higher in Guanabara Bay than in those Sepetiba and Paraty Bays; however, the same pattern was not reported between Sepetiba and Paraty Bays. According to Azevedo and Van Sluys (2005) and Rossi-Santos and Podos (2006), start and minimum frequencies of Guiana dolphin whistles increase from south to north in Brazil, and our study provided some corroborative evidence for this pattern. However, the whistle variations found in our study may be related to adaptation to ecological conditions.

Guiana dolphins in Guanabara Bay emitted shorter, higher frequency whistles than individuals in Sepetiba and Paraty Bays. The mean frequency of Guiana dolphin whistles from Guanabara Bay was 2.11 kHz higher than the mean frequency from Sepetiba Bay and 3.46 kHz higher than the mean frequency from Paraty Bay, respectively. The mean duration of whistles from Guanabara Bay was 87 ms shorter than the mean duration from Sepetiba Bay and 104 ms shorter than mean duration from Paraty Bay. These finding may be related to the acoustic characteristics of the environments, since Guanabara Bay has the most intense boat traffic of the three study areas.

Dolphins in this bay seem to be exposed to louder ambient noise than those in Sepetiba and Paraty Bays. Some studies attributed variation in whistle parameters to ambient noise (Van Parijs and Corkeron 2001; Buckstaff 2004; Morisaka et al. 2005; Ansmann et al. 2007; May-Collado and Wartzok 2008). For example, frequency parameters of common dolphin (Delphinus delphis) whistles were higher in habitats with high

48

48

48

This study (n=234) 48 kHz Sepetiba Bay, Brazil

This study (n=222) 48 kHz Paraty Bay, Brazil

–

Mx.F (kHz)

–

8.16±3.0 14.35±3.0 7.97±2.89 14.46±2.88 (1.0–16.0) (2.0–18) (1.0–15.80) (2.2–17.90) 13.83±6.16 19.51±6.36 12.31±5.16 21.21±5.82 (1.13–47.36) (1.52–47.36) (1.38–35.75) (3.0–48.40)

6.48±3.0 (1.0–16.0) 9.02±5.71 (0.95–29.30)

19.05±2.97 9.83±4.03 (9.23–23.89) (0.21–22.20)

–

–

Frequency of ½

–

13.82±3.58 (5.7–23.4)

–

15.99±3.43 (7.4–23.6)

15.36±6.44 (2.05–21.70)

–

–

Frequency of ¾

11.32±3.80 15.02±5.21 19.27±5.20 (2.43–28.59) (3.09–34.78) (4.21–40.78) 10.29±2.94 13.00±4.34 16.72±6.07 (3.65–20.15) (4.21–28.68) (4.22–33.00)

360.05±135.62 7.93±2.47 23.42±7.78 7.77±2.32 23.68±7.76 15.91±7.87 (54–826) (1.87–16.40) (4.31–44.90) (1.87–15.46) (4.31–44.90) (0.47–41.71) 7.74±2.20 22.33±7.94 14.56±8.30 376.80±159.78 8.09±2.49 22.26±7.99 (1.03–14.53) (4.59–42.84) (0.65–35.52) (53–1,231) (1.03–17.71) (4.59–42.84)

12.79±3.74 16.54±4.80 20.96±6.07 (5.72–30.37) (7.03–30.93) (7.78–35.34)

15.37±5.35 16.60±5.33 17.60±5.36 (1.10–39.06) (1.13–37.60) (5.37–21.97)

–

11.73±3.53 (3.9–21.7)

11.11±4.72 13.66±6.18 (2.74–12.07) (2.33–15.11)

–

–

Delta Frequency Frequency (kHz) of ¼

7.6±2.9 13.0±4.1 – (0.5–16.5) (1.6–18.0) 10.52±4.51 13.31±4.85 7.05±12.08 (1.03–10.98) (1.17–17.49) (1–7.21)

0.3

Mn.F (kHz)

18.82±3.10 9.22±3.44 9.57±3.76 (9.23–23.75) (1.34–20.3) (1.34–21.93)

12.8±4.5 (0.5–18.0) 13.31±5.86 (3.2–16.83)

–

EF (kHz)

272.44±105.25 9.88±3.90 25.58±7.38 9.52±3.55 25.79±7.51 16.52±7.81 (46–652) (2.15–26.53) (8.90–42.65) (2.15–25.40) (8.90–42.65) (0.84–34.78)

229±109.9 (38–627) 200±187 (7–1,027)

18

200–250

308±137.3 (38–1,064)

7.9±2.9 (0.9–17.9) 10.70±4.97 (1.03–11.06)

102.5±81 (10–852) 789±3.11 (9–2,282)

24

This study (n=203) Guanabara Bay, Brazil

Azevedo and Van Sluys (2005) (n=696) southern and northern areas, Brazil Pivari and Rosso (2005) (n=2,094) Cananéia, Brazil May-Collado and Wartzok (2009) (n=422) Costa Rica

–

SF (kHz)

210±20

Recording Duration (ms) bandwidth (kHz)

Monteiro Filho and Monteiro (2001) 8 (n=214) Cananéia, Brazil Azevedo and Simão (2002) (n=5,086) 18 Guanabara Bay, Brazil Erber and Simão (2004) (n=3,350) 24 Sepetiba Bay, Brazil

Studies

Whistle parameters

Table 5 Descriptive statistics with n=whistle sample size, mean values±standard deviation, and frequency range of whistle parameters for Guyana dolphins from previous studies in Brazil and Costa Rica with different recording bandwidth and from this study in three areas of southeastern Brazil (Guanabara, Sepetiba, and Paraty Bays). Frequency parameters are in kHz and duration in ms

acta ethol

acta ethol

ambient noise (Ansmann et al. 2007). The authors suggested that common dolphins in the English Channel may have shifted the frequencies of their vocalizations upward to avoid masking by low-frequency ambient noise produced by high levels of vessel traffic in this area. May-Collado and Wartzok (2008) found that whistles emitted by bottlenose dolphin (Tursiops truncatus) had a higher maximum frequency and were longer in duration in areas with high ambient noise.

Significant differences were also found in ascending (the most common whistle type in all three areas), descending– ascending, and multi whistles recorded between Guanabara Bay and the other two areas. The analysis of the acoustic parameters of the whistles for each contour form provides a more accurate comparison of these sound emissions.

Although the ascending whistles from these distinct areas showed the same contour form, they have differences in their acoustic parameters. Differences found between the same contour forms in different areas might be related to individual characteristics such as the emission of signature whistles.

Different types of whistles may be linked to individual recognition and may serve to maintain contact between individuals (Caldwell et al. 1990; Janik and Sayigh 2013). Each dolphin develops its own unique frequency modulation pattern as an individually distinctive signature whistle (Caldwell et al.

1990, Janik and Slater 1998). One study of Guiana dolphin whistles in Sepetiba Bay reported 27 distinct types of whistles and suggests the possible occurrence of signature whistles (Figueiredo and Simão 2009). A finer whistle categorization of this species is needed to investigate individual characteristics and the possible presence of signature whistles. Future studies using categorization methods such as ARTWARP (Deecke & Janik 2006) in combination with SIGID (Janik et al. 2013) are important to explore the possible existence of signature whistles in Guiana dolphin. These authors developed novel methods for the categorization of bioacoustic signals and the identification of signature whistles, respectively (Deecke & Janik 2006; Janik et al. 2013).

Our findings illustrate the value of a broadband recording system in bioacoustic studies of Guiana dolphins. The use of such a system in our study allowed for the detection of differences in whistles in adjacent dolphin populations.

May-Collado and Wartzok (2009) observed that frequency range was responsible for 89 % of the variation found in comparisons of Guiana dolphin whistles among different studies. By doubling the sampling rate in our recording system, we were able to more accurately sample the whistle repertoire of Guiana dolphins in southeastern in Brazil, and thereby detect differences in whistles between neighboring populations.

Acknowledgments This study was supported by a technical cooperation grant between Petrobras, UERJ, and ACPNR (4600–271434), as well as from Cetacean Society International (CSI). The authors thank the

School of Oceanography (FAOC, UERJ) for logistical support. We also thank engineer Orlando de Jesus Ribeiro Afonso from the Brazilian Navy Research Institute (IPqM) for technical support. The authors thank the Graduate Program of Ecology and Evolution (PPGEE, UERJ) for support. We particularly thank Régis Pinto de Lima, Adriana Nascimento Gomes, Sylvia Chada, and Sílvia Peixoto from the Tamoios Ecological Station (ESEC Tamoios-ICMBio) for fieldwork logistics in Paraty Bay. This study was partially funded by the Brazilian Research Council (CNPq-Brazil; Edital Universal No. 476255/2007-4). Dr. Azevedo has a research grant from CNPq (grant No. 304826/2008-1). Dr. Lailson-Brito is a researcher of “Prociência” Program—FAPERJ/UERJ. Thanks to researchers and students of the Aquatic Mammal and Bioindicator Laboratory (MAQUA, UERJ).

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