Whistle vocalizations of Indo-Pacific bottlenose (Tursiops aduncus) inhabiting the south-west Indian Ocean

Tess Gridleya) Sea Research Unit, School of Biology, University of St. Andrews, St. Andrews, Fife, KY16 8LB, United Kingdom

Per Berggren School of Marine Science and Technology, Newcastle University, Tyne and Wear, NE1 7RU, United Kingdom

Victor G. Cockcroft Centre for Studies, Department of Zoology, Nelson Mandela Metropolitan University, Port Elizabeth, Eastern Cape, 6031, South Africa

Vincent M. Janik Sea Mammal Research Unit, School of Biology, University of St. Andrews, St. Andrews, Fife, KY16 8LB, United Kingdom (Received 26 April 2012; revised 6 September 2012; accepted 4 October 2012) Populations of Indo-Pacific (Tursiops aduncus) are distributed along coastal regions of the south-west Indian Ocean (SWIO), from South Africa to Kenya. An account of whistles from wild T. aduncus inhabiting the SWIO is provided here. Recordings were made at Plettenberg Bay (South Africa) and Zanzibar Island (Tanzania) and the frequency trace of whistle contours (n ¼ 1677) was extracted. Multiple parameters were measured from each whistle and compared between regions and encounters. Regional variation was significant in all parameters assessed except for start and middle frequency (frequency at half the duration). Whistles from Zanzibar Island ended on average 4 kHz higher than those from Plettenberg Bay, and had a steeper frequency gradient. However, mean frequencies differed by <1 kHz and population averages for the adopted frequency distribution showed similar patterns, with a peak between 5 and 7 kHz. Whistle parameters were strongly influenced by recording encounter, likely reflecting the presence of different individuals, group compositions and behavioral contexts during recording occasions. Comparisons within the genus showed that T. aduncus from the SWIO have amongst the lowest start and minimum frequency of whistles within Tursiops. VC 2012 Acoustical Society of America. [http://dx.doi.org/10.1121/1.4763990] PACS number(s): 43.80.Ka [WWA] Pages: 4032–4040

I. INTRODUCTION S€arnblad et al., 2011). However, for the purposes of this study, we accept the designation of three Tursiops species: The bottlenose dolphin (Tursiops spp.) is one of the best the common bottlenose dolphin, T. truncatus, the Indo- studied of all the . However, there remains continued Pacific bottlenose dolphin, T. aduncus (LeDuc et al., 1999), debate surrounding the number of Tursiops species to be rec- and the newly recognized Australian bottlenose dolphin, ognized and the phylogenetic relationships between popula- T. australis (Charlton-Robb et al., 2011), along with the sub- tions for which we have genetic information (Natoli et al., species T. truncatus ponticus from the Black Sea (Viaud- 2004; Viaud-Martinez et al., 2008; Charlton-Robb et al., Martinez et al., 2008). 2011; S€arnblad et al., 2011). There is growing evidence that There are few reports of T. aduncus vocalizations and Tursiops is polyphyletic, with T. aduncus from some popula- no published data from wild inhabiting the SWIO tions having a closer relationship to and Delphinus region. Like T. truncatus, the vocal repertoire of T. aduncus than to T. truncatus (LeDuc et al., 1999; Natoli et al., 2004). includes whistles and echolocation clicks (Tietz and Tayler, Based on mtDNA markers, T. aduncus from the south-west 1964; Morisaka et al., 2005b; Hawkins, 2010). The only Indian Ocean (SWIO) may represent an independent lineage account of the vocal behavior of T. aduncus from the SWIO from Chinese T. aduncus animals and be more closely originates from a captive facility in South Africa. This dates related to T. truncatus from regions in Asia and the NW from 1964 (Tietz and Tayler, 1964) and focuses on two ani- Atlantic (Gridley, 2011; S€arnblad et al., 2011). With further mals that produced whistles ranging from 2 to 14 kHz and investigation, this may warrant classification of Chinese being, on average, 1.064 s in duration. T. aduncus and probably Australian T. aduncus (Moller€ and We report on the whistle characteristics of T. aduncus Beheregaray, 2001) as a separate species (Natoli et al., 2004; from two coastal regions of the SWIO, Plettenberg Bay in South Africa and the Island of Zanzibar, Tanzania. In both a)Author to whom correspondence should be addressed. Electronic mail: locations, coastal populations of T. aduncus (usually in [email protected] water <50 m deep) are parapatric with offshore populations

4032 J. Acoust. Soc. Am. 132 (6), December 2012 0001-4966/2012/132(6)/4032/9/$30.00 VC 2012 Acoustical Society of America Author's complimentary copy of T. truncatus (Ross et al., 1987; Amir et al., 2005; 100 m of each other. Whenever a group was located, an Best, 2007). In many ways, the demographics of these popu- encounter was begun and standard information on the esti- lations are sharply contrasting. The population size of mated group size and presence or absence of calves was T. aduncus along the southern coast of South Africa includ- documented. If two or more groups joined, the join time was ing Plettenberg Bay is in the region of 16 220–40 744 indi- noted and a new encounter was begun. Each encounter began viduals (Reisinger and Karczmarski, 2010) with the dolphins with a period of photo-identification to determine the indi- passing through Plettenberg Bay considered somewhat mi- viduals present and was followed by a period of acoustic gratory and traveling in characteristically large group sizes data collection using the equipment summarized in Table I. averaging 140 individuals (Saayman and Tayler, 1973). Sympatric populations of whistling delphinids exist in both Although the population is large, there is low genetic diver- regions (principally those from the genus Sousa and Delphi- sity amongst coastal stocks of South African T. aduncus nus)(Amir et al., 2005; Best, 2007). Only encounters of sin- (Natoli et al., 2007; Gridley, 2011). In Zanzibar, the esti- gle species groups of T. aduncus were used in this analysis. mated population size off the south coast of the island in Data were collected during a variety of behavioral contexts 2007 was 212 individuals (95% CI 163–260) and in 2008 off including feeding, resting, socializing, milling and traveling. the north coast 254 (95% CI 199–460) (Berggren, 2011). Photo-identification data document mixing of individuals Molecular mtDNA analysis has identified significant struc- between north and south Zanzibar (Berggren, 2011). There- turing between T. aduncus to the north and the south fore, for the purpose of acoustical analysis we have com- of Zanzibar Island [FST ¼ 0.19, p ¼ 0.002; uST ¼ 0.31, bined recordings from coastal Zanzibar and treat the island p < 0.001 (S€arnblad et al., 2011)], indicating limited genetic as a single region. exchange between these geographically neighboring loca- We use the term “whistle” to describe a narrow band tions. This differentiation is considerably higher than that tonal signal with at least part of the fundamental frequency between southern Zanzibar and South Africa, suggesting above 3 kHz. This distinguishes whistles from narrow band a common founder population or recent range expansion low-frequency sounds produced by bottlenose dolphins linking these areas (S€arnblad et al., 2011). However, photo- (Simrad et al., 2012). Only whistles longer than 0.1 s were identification reveals temporary movement of resident indi- analyzed (Janik et al., 2012) and harmonics other than the viduals between the south and northern localities (Berggren, fundamental were not considered. Whistles interrupted by 2011) indicative of ecological intermixing between these very short breaks (<0.03 s) were considered as continuous, two regions. but no attempt was made to identify disconnected multi- Here we provide the first description of the whistles pro- loops (Esch et al., 2009; Janik et al., 2012) or signature duced by wild, free-ranging T. aduncus from the SWIO and whistles (Caldwell et al., 1990). Whistle contours (the modu- compare the whistle parameters to those of multiple Tursiops lation pattern of the fundamental frequency) were extracted populations. as a series of frequency measurements at 5 ms intervals along the fundamental frequency. To do this, contours were initially visualized in the spectrogram display of Adobe II. METHODS AUDITION v2.0 (Hanning window, FFT resolution 512). Each Acoustic recordings were made from groups of dolphins was visually assessed and graded based on the signal-to-noise passing through the inshore waters of Plettenberg Bay (PB), ratio (1: signal is faint and barely visible on the spectrogram, South Africa (34.0185S, 23.4197E) and at two sites sepa- 2: signal is clear and unambiguous, 3: signal is prominent and rated by 80 km north and south of Zanzibar Island (ZB), dominates). Extractable contours were those graded as 2 or 3, Tanzania (north Zanzibar, 5.7682S, 39.3546E and south which had a clear start and end point and overall shape, were Zanzibar, 6.4417S, 39.4575E). Molecular analysis has unmasked and not cut off by the frequency bandwidth of the confirmed that coastal bottlenose dolphins in both PB and ZB recording system. As different recording equipment was used are T. aduncus (Natoli et al.,2004; S€arnblad et al., 2011). at each location (Table I), the number of contours that were Boat surveys were carried out to locate dolphins and bandwidth limited was counted for each region to assess the conduct focal follows (Altmann, 1974) of groups (see Table I influence of the Nyquist frequency on the end and maximum for details). Groups were defined as all individuals within frequency of whistle contours. The fundamental frequency of

TABLE I. Summary details of acoustic data collection from two populations of T. aduncus.

Population (collection date) Research vessel Method (depth in m) Hydrophone model Recording medium Sampling rate Frequency response

Plettenberg Bay 6.3 m fiberglass boat (a) Towed from (a) HTI-96-MIN (a) Edirol UA-25 (a) 96 kHz (a) 2 Hz to 30 kHz (March 2009) powered by 2 85 hp boat (2 m) sound card to PC (61 dB) outboard engines (b) Stationary from (b) Magrec HP/30 (b) Edirol R1 (b) 44.1 kHz (b) 200 Hz to 15 kHz boat (2.5 m) General Purpose (61.5 dB) Zanzibar Island 5 m aluminum boat Stationary from HTI-96-MIN Edirol UA-25 sound 96 kHz 2 Hz to 30 kHz (February–March 2008) powered by either a boat (6 m) card to PC (61 dB) 40 or 80 hp outboard engine

J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins 4033 Author's complimentary copy each contour was automatically extracted using a supervised (n ¼ 3847) were. Extracted contours were analyzed from 29 peak function in MATLAB v 6.5.1, which allowed manual cor- encounters (PB n ¼ 511 contours from 10 encounters, ZB rection when needed [display settings: fast Fourier transform n ¼ 1157 contours from 19 encounters) and one occasion (FFT) size 2048, 512 frame length, 87.5% overlap and a from Zanzibar where groups joined (n ¼ 9). On average 58 Hanning window]. (6SD 61) whistle contours were extracted from each en- Contour parameters were automatically measured from counter. Median and mean (6SD) group sizes during record- extracted contours using purpose written MATLAB script that ings were 150 and 156 (6SD 82) individuals in Plettenberg was developed and tested on whistles from multiple Tursiops Bay and 30 and 28 (6SD 11) individuals in ZB, respec- spp. populations (Gridley, 2011). We report the values of dis- tively. The presence of calves was confirmed in 9 out of 10 crete frequency (kHz) parameters; start, end, minimum, and encounters in Plettenberg, 15 out of 19 encounters in Zanzi- maximum, the frequency at the first, middle, and third quartiles bar and during the group join. of duration, the frequency range, and mean frequency (average A selection of representative contours from each popu- of all the frequency points making up the contour at 5 ms reso- lation is shown in Fig. 1. After applying a Bonferroni correc- lution). Additional parameters included the frequency change tion there was regional variation in all whistle contour (difference between the end and start frequency), absolute parameters assessed apart from start and middle frequency frequency gradient [absolute value of (end frequency start (Mann-Whitney U test: start frequency p ¼ 0.006, middle fre- frequency)/contour duration], number of inflection points and quency p ¼ 0.100, all others p < 0.001, n1 ¼ 511, n2 ¼ 1166). duration (s). The adopted frequency (Morisaka et al., 2005a) Most notably, the whistle contours of T. aduncus from ZB of each whistle contour was calculated as the proportion of the had a higher end frequency (x ZB ¼ 11.44 kHz 6 SD 4.30, contour which falls into 1 kHz frequency bins, therefore meas- coefficient of variation (CV) 37.56, x PB ¼ 6.98 kHz 6 SD uring the distribution of the signal in different frequencies. Pa- 4.26, CV 60.94) and maximum frequency (x ZB rameters were chosen for consistency with previous studies ¼ 12.10 kHz 6 SD 3.91, CV 32.32, x PB ¼ 9.62 kHz 6 SD (Oswald et al., 2003; Morisaka et al., 2005a,b; Ansmann et al., 3.21, CV 33.38) compared to PB (Table II,Fig.2). This trend 2007; Dıaz Lopez, 2011). remained when we consider just the contours recorded in For both regions, the parameter data were non-normally PB using the HTI (High Tech, Inc.) hydrophone with a distributed (Wilk-Shapiro test: p < 0.05) and in most cases the frequency response to 48 kHz (x end frequency PB variance within populations was non-homogenous (Levene’s HTI ¼ 7.30 kHz 6 SD 4.22, x maximum frequency PB tests of equal variances: p < 0.05). Differences between the HTI ¼ 9.79 kHz 6 SD 2.97, n ¼ 216, Mann-Whitney U test contour parameters and selected adopted frequency bands between PB HTI and ZB significant at p < 0.001 for both pa- (5, 10, and 15 kHz) of the two regions were therefore deter- rameters) demonstrating that the differences observed are not mined using non-parametric Mann-Whitney U tests. Bonfer- an artifact of the two different recording systems used. In both roni correction was applied to the a value to prevent error due regions, the start and minimum frequency were positively cor- to multiple pairwise comparisons between the populations for related (Pearson’s correlation PB: r ¼ 0.56, p < 0.001, ZB: the whistle contour characteristics (n ¼ 13 comparisons) and r ¼ 0.64, p < 0.001), as were the end and maximum frequency adopted frequencies (n ¼ 3 comparisons), i.e., a with Bonfer- (PB: r ¼ 0.69, p < 0.001, ZB: r ¼ 0.90, p < 0.001). roni correction is 0.05/16 comparisons ¼ 0.003. The whistle contours from Zanzibar Island had a steep We conducted a nested (cf. hierarchical) analysis of var- absolute gradient (x¼ 18.77 kHz/s 6 SD 13.62) and generally iance (ANOVA) to understand the importance of recording inclined with an average net increase of 5.55 kHz (6 SD 5.08) encounter on variation in whistle parameters. The magnitude over the duration of the call (Fig. 2). Although the contours of variance components was estimated with region and en- from PB also generally increased in frequency over time, the counter as the first and second random factors and parameter gradient was less steep (x ¼ 8.76 kHz/s 6 SD 9.06) and the data as the response variable. For brevity, the middle and net change in frequency was lower than seen in ZB inter-quartile frequency parameters were omitted from this (x ¼ 1.45 kHz 6 SD 4.18). The whistle contours of T. aduncus analysis. As the response data violated the assumptions from PB were slightly longer than those of ZB (x duration of parametric ANOVA we applied a rank transformation PB ¼ 0.44 s 6 SD 0.28, CV 62.25, x ZB 0.37 s 6 SD 0.22, CV (Conover and Iman, 1981), whereby each value was con- 58.99) and the contours slightly more inflected, although in verted to a rank score from 1 to n (tied scores were assigned both regions the number of inflection points was low, mostly 0 an average value) and analysis was conducted on the ranked or 1 (Fig. 2). data (Quinn and Keough, 2002). Nine whistle contours from Although there were key differences in the frequency pa- ZB recorded during a join of two groups were removed from rameters considered, the mean frequency of contours from the this analysis as they bridged encounters. two regions differed by less than 1 kHz (x PB ¼ 6.41 kHz 6 SD 1.58, CV 24.65, x ZB ¼ 7.32 kHz 6 SD 1.81, CV 24.71). Re- gional averages of the adopted frequency distributions were III. RESULTS similar (Fig. 3), with a clear peak between 5 and 7 kHz in both In total more than 5236 whistle contours were identified regions and no appreciable variation in the 5 kHz adopted fre- from recordings of T. aduncus, of which 1677 were of a high quency band (Mann-Whitney U test p ¼ 0.009). However, var- enough quality for the frequency contour to be extracted. iationinthefrequencybandsat10and15kHzwasapparent Only one of the 1389 whistle contours identified from PB (Mann-Whitney U test p < 0.001 for both) with the bandwidth was bandwidth limited, and none of the contours from ZB of whistle contours from ZB being slightly greater than those

4034 J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins Author's complimentary copy FIG. 1. Example whistles from Plettenberg Bay (a)–(d) and Zanzibar Island (e)–(h). of PB (x frequency range ZB ¼ 7.74 kHz 6 SD 4.01, CV tance of encounter in the analysis (ANOVA with encounter 51.86, x PB ¼ 5.70 kHz 6 SD 3.44, CV 60.47) (Figs. 2 and 3). nested in region, df27,1639, p < 0.001 for all parameters). A high degree of variation in the adopted frequency suggested Regional variation was greater than that observed between variation between individuals in this parameter. encounters only for end frequency (35.16%), frequency Examination of the magnitudes of variance components change (28.82%) and frequency gradient (25.89%). Relative (Table II) from the nested ANOVA highlights the impor- to regional variance, between encounter variance

J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins 4035 Author's complimentary copy TABLE II. Examination of the effect of encounter on the variation in whistle parameters between regions (Plettenberg Bay and Zanzibar Island).a

Between encounter Within encounter Whistle parameter Fit of model Region (DF 1) (DF 27) (DF 1639)

Start frequency R2 0.20 F 9.17 15.89

F28,1639 15.65 %V 0.00 21.68 78.32 P 0.002 < 0.001 End frequency R2 0.36 F 518.35 15.93

F28,1639 33.87 %V 35.16 14.08 50.76 Minimum frequency R2 0.26 F 111.41 18.11

F28,1639 21.44 %V 7.91 22.22 69.87 Maximum frequency R2 0.30 F 248.19 17.71

F28,1639 25.94 %V 18.98 19.20 61.82 Frequency range R2 0.22 F 137.17 13.26

F28,1639 17.69 %V 11.62 16.41 71.97 Mean frequency R2 0.31 F 154.20 22.43

F28,1639 27.13 %V 10.42 25.52 64.06 Frequency change R2 0.25 F 345.68 9.12

F28,1639 21.14 %V 28.82 9.34 61.84 Frequency gradient R2 0.23 F 294.64 8.21

F28,1639 18.44 %V 25.89 8.76 65.35 Inflection points R2 0.09 F 51.64 5.35

F28,1639 7.00 %V 5.31 7.08 87.61 Duration R2 0.13 F 33.51 9.20

F28,1639 10.06 %V 2.16 12.94 84.90 aResults of nested ANOVA performed on ranked data with encounter nested in region. Unless otherwise stated, p < 0.001 for all comparisons. DF ¼ degrees of freedom, V ¼ variance component calculated as percentage of the total. components were relatively high for mean, minimum and onstrate geographic variation between the two study regions start frequency (25.52%, 22.22%, and 21.68%, respectively). in most of the whistle parameters assessed. Whistle contours However, in all instances the magnitude of variance within from ZB had a steeper gradient and more positive aspect and encounter was the greatest, ranging from 50.76% to 87.61%. usually ended around 4 kHz higher in frequency than those from PB (Fig. 2). However, the overall distribution of IV. DISCUSSION adopted frequencies used was strikingly similar between the two regions and mean frequency, which was the least vari- We present the first description of the whistle contours able parameter in both populations, differed by less than produced by T. aduncus inhabiting African waters and dem- 1 kHz. The contours from both regions were fairly simplistic in shape, characterized by few or no inflection points, which

FIG. 2. Average (6SD) whistle parameters from T. aduncus in Plettenberg FIG. 3. Adopted frequency distribution of whistle contours produced by Bay and Zanzibar Island. Note y axis with frequency parameters (kHz) T. aduncus from Plettenberg Bay and Zanzibar Island. Calculated as the pro- shown to the left of the dotted line, and number of inflections and duration portion of the total contour duration within 1 kHz frequency bins and aver- to the right. *Unit for frequency gradient is kHz/s. aged over all the contours from each population.

4036 J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins Author's complimentary copy for ZB, in particular, was reflected by a predominance of up- frequencies ranging up to 75 kHz (Samarra et al., 2010). swept whistle contours (Fig. 1). Whistle parameters were May-Collado et al. (2007a) suggest that call frequency char- strongly influenced by recording encounter and the variance acteristics and social group structure may be linked, with component within encounter was high for all parameters. minimum frequency higher in species with large group sizes. Tursiops aduncus from the SWIO are more closely Our data do not support this as here we document a less than related to each other than to T. aduncus in the western Pa- 0.5 kHz difference in the minimum frequency of whistles cific Ocean (S€arnblad et al., 2011) and may represent a sep- from two regions where group sizes are at the limits of that arate lineage from Austral-Asian populations (Natoli et al., observed in the Tursiops genus (Stensland et al., 2006; 2004). Of the frequency parameters considered, the trends Reisinger and Karczmarski, 2010). There are consistent dif- in the start and minimum frequency best reflect the pattern ferences in the cranial length and morphology of T. truncatus of intra-specific genetic differentiation in T. aduncus, per- and T. aduncus (Hale et al., 2000; Kurihara and Oda, 2007). haps indicating an influence of genetic factors (or factors We suggest that differences in the frequency parameters of correlated with genetic differentiation) on these parameters. these species may be related to differences in the sound The number of inflections and duration of whistle contours production structures, such as morphological variation asso- from the SWIO were highly variable, supporting previous ciated with cranial characteristics at the source of sound observations of other Tursiops populations (Steiner, 1981; production, the monkey lips/dorsal bursae (Cranford et al., Wang et al., 1995; Oswald et al., 2003; Morisaka et al., 1996) or differences in the basal part of the rostrum (Kuri- 2005b) indicating that identity or motivational cues might hara and Oda, 2007). However, this possibility requires em- be encoded in these characteristics (Janik et al., 1994). pirical testing. The whistle contour frequency parameters from this Several dolphin species use individually distinctive sig- study and other Tursiops populations are summarized in nature whistles, most prominently T. truncatus (Caldwell Table III. Comparisons within T. aduncus demonstrate that et al.,1990; Janik, 2009). Key similarities in the social or- the whistle contours of this species have broadly similar start ganization, behavior and ecology of T. aduncus and the and minimum frequencies, ranging on average from 5.53 to coastal form of T. truncatus, combined with their genetic 7.17 kHz and from 3.92 to 5.98 kHz for start and minimum, relatedness suggest that T. aduncus may use signature whis- respectively. The magnitude of geographic variation is far tles to communicate identity information (Gridley, 2011). greater in the end, maximum frequency and inflection points. However, this has yet to be demonstrated conclusively in In describing the contours from PB we are documenting the captive or wild populations and the ability for vocal produc- lowest of any T. aduncus populations for start, end and mini- tion learning, the process by which signature whistles are mum whistle frequency and amongst the lowest for the max- developed (Sayigh and Janik, 2010), has still to be shown. imum frequency. In ZB, the start and minimum frequency Signature whistles are often composed of repeated series of were comparatively low, but this region had the highest end short contours, termed loops, separated by up to 0.25 s of frequency of all T. aduncus populations considered. The con- silence (Janik and Slater, 1998; Esch et al.,2009). Deci- tours of T. aduncus were usually less than 1 s in duration and phering disconnected multi-looped signature whistles in those from the SWIO were amongst the shortest docu- populations with high whistle rates requires careful catego- mented, lasting on average less than half a second. rization and bout analysis (Janik et al.,2012). As the objec- As previously noted by Hawkins (2010), the frequency tive of this study was to present the first account of whistle parameters of T. aduncus are generally much lower than contours produced by T. aduncus in the SWIO, we did not T. truncatus, particularly with respect to the start, minimum investigate the functionally different call types. However, and maximum frequencies used. The whistle contours from as signature whistles represent around 50% of the whistles T. aduncus also tend to be shorter in duration than those of emitted by freely interacting bottlenose dolphins (Cook T. truncatus, although methodological differences between et al., 2004; Sayigh and Janik, 2010) and occur in bouts studies in defining whistle contours may also influence this (Janik et al., 2012), the high variance components within parameter. The inter-specific variation in whistle parameters encounters may reflect the presence of different individuals cannot be readily explained by differences in the social producing their signature whistles in bouts. Behavioral con- structure or habitat preference of T. aduncus and the coastal text and group composition, including the presence or ab- form of T. truncatus, as these do not vary consistently sence of calves is also likely to influence the proportion of between the species (Scott et al., 1990; Moller€ and Harcourt, signature whistles to non-signature whistles and the fre- 1998; Connor et al., 2000; Moller€ et al., 2007). Being the quency of contours produced (Janik and Slater, 1998; Cook smaller of the two species (Hale et al., 2000), the lower et al., 2004; Morisaka et al.,2005c; Janik et al.,2012). The whistle contour frequencies produced by T. aduncus are not significance of encounter in our analysis therefore demon- consistent with expectations of body size (May-Collado strates that any attempt to classify animals to species using et al., 2007b). However, the relationship between body whistle vocalizations must be developed with thorough length and call frequency, which transcends taxonomic sampling of groups and individuals over multiple encoun- divides (Badyaev and Leaf, 1997; Bertelli and Tubaro, 2002; ters to adequately capture the whistle repertoire. Regional May-Collado et al., 2007b) becomes less strong when phylo- variation in whistle parameters demonstrates that detection genetic relationships are taken into account (May-Collado algorithms used in passive acoustic monitoring must be ro- et al., 2007b) and recent evidence shows that killer whales, bust to regional variation in call types or trained using loca- the largest delphinid, produce whistles with fundamental tion specific data.

J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins 4037 Author's complimentary copy 08J cut o.A. o.12 o ,Dcme 02Gridley 2012 December 6, No. 132, Vol. Am., Soc. Acoust. J. 4038

TABLE III. Summary of key acoustic parameters (x 6 SD) of whistle contours (n, unless otherwise indicated) from Tursiops populations.

Location n Start frequency (kHz) End frequency (kHz) Minimum frequency (kHz) Maximum frequency (kHz) Inflection points (n) Duration (s) Source

Tursiops aduncus Plettenberg Bay, South Africa 511 5.53 (2.86) 6.98 (4.26) 3.92 (1.64) 9.62 (3.21) 0.66 (0.88) 0.44 (0.28) This study Zanzibar, Tanzania 1166 5.89 (3.08) 11.44 (4.30) 4.37 (1.35) 12.10 (3.91) 0.42 (0.77) 0.37 (0.22) This study Amakura-Shimoshima I’s., Japan 515 6.74 (2.82) 8.06 (3.80) 5.63 (2.21) 9.39 (3.90) 0.78 (0.88) 0.37 (0.25) Morisaka et al., 2005b Mikura I., Japan 851 7.17 (2.85) 9.82 (4.18) 5.98 (2.44) 12.21 (3.20) 1.22 (1.39) 0.39 (0.33) Morisaka et al., 2005b Ogaswaea I’s., Japan 247 6.91 (3.12) 10.35 (4.86) 5.61 (2.06) 12.34 (4.93) 1.19 (1.50) 0.44 (0.44) Morisaka et al., 2005b Bunbury, Australia 5178 5.95 (1.93) 9.43(3.59) 4.63 (1.24) 10.92 (3.76) 2.09 (2.01) 0.71 (0.34) Hawkins et al., 2010a Morton Bay, Australia 1842 6.16 (3.75) 7.58 (4.00) 4.86 (1.50) 11.67 (3.23) 1.73 (1.44) 0.50 (0.32) Hawkins et al., 2010a Byron Bay, Australia 1930 6.40 (3.48) 8.87 (4.05) 5.31 (2.35) 13.05 (4.38) 2.07 (2.02) 1.11 (0.81) Hawkins et al., 2010a Tursiops truncatus Galveston, TX 811 7.95 (2.88) 9.02 (3.96) 5.98 (2.30) 11.95 (3.08) 2.57 (2.62) 0.75 (0.46) Wang et al., 1995 Corpus Christi, TX 617 7.43 (2.44) 8.71 (4.04) 5.88 (2.65) 11.43 (3.80) 2.14 (2.97) 0.69 (0.41) Wang et al., 1995 South Padre Island, TX 549 8.70 (2.95) 6.40 (2.44) 5.37 (1.12) 10.33 (2.80) 1.37 (1.65) 0.60 (0.26) Wang et al., 1995 a Gulf of Mexico 26g 10.82 (1.78) 11.17 (2.71) 7.87 (1.01) 16.19 (2.06) 3.02 (n/a) 0.88 (0.26) Baron et al., 2008 Gandoca-Manzanillo, Costa Rica 77 8.43 (3.66) 13.15 (5.57) 5.68 (2.24) 17.61 (4.93) 2.64 (3.41) 0.89 (0.69) May-Collado and Wartzok 2008 Bocas del Toro, Panama 74 9.10 (3.70) 9.19 (4.27) 5.34 (1.90) 15.34 (3.65) 3.78 (4.11) 1.10 (0.74) May-Collado and Wartzok 2008 W. N Atlantic 858 11.26 (3.99) 10.23 (3.65) 7.33 (1.66) 16.24 (2.69) 2.86 (2.45) 1.30 (0.63) Steiner, 1981 a W. N Atlantic 21g 10.64 (2.53) 12.40 (2.80) 8.24 (1.85) 15.03 (2.80) 1.43 (n/a) 0.62 (0.27) Baron et al., 2008 tal. et Patos Lagoon Estuary, S. Brazil 788 8.28 (3.11) 8.37 (3.70) 5.96 (2.15) 12.21 (3.20) 1.42 (1.85) 0.55 (0.39) Azevedo et al., 2007

hslso noPcfcbtlns dolphins bottlenose Indo-Pacific of Whistles : Golfo de San Jose, Argentina 110 9.24 (2.74) 6.63 (2.29) 5.91 (1.50) 13.65 (1.54) 1.58 (1.24) 1.14 (0.49) Wang et al., 1995 Sado Estuary, Portugal 735 5.80 (1.80) 12.10 (4.40) 5.40 (1.20) 15.00 (2.70) n/a 0.86 (0.40) dos Santos et al., 2005 Sardinia, Italy 600 9.07 (4.24) 11.36 (6.64) 7.86 (3.65) 13.09 (5.44) 1.6 (2.45) 0.62 (0.76) Dıaz Lopez 2011a North Pacific 306 11.61 (5.11) 10.24 (4.78) 7.92 (2.49) 17.07 (4.55) 2.85 (2.67) 1.11 (0.69) Oswald et al., 2007 Gulf of California 110 12.10 (2.89) 9.19 (3.44) 6.91 (2.11) 13.68 (1.72) 1.15 (1.32) 0.66 (0.35) Wang et al., 1995

a Standard deviations acquired through personal communication with the author. ng Sampling unit is group. Author's complimentary copy V. CONCLUSIONS Connor, P. L. Tyack, and H. Whitehead (The University of Chicago Press, Chicago), pp. 91–126. This is the first report of bottlenose dolphin vocaliza- Conover, W. J., and Iman, R. L. (1981). “Rank transformations as a bridge tions from animals inhabiting African waters and we have between parametric and non-parametric statistics,” Am. Stat. 35, 124–129. Cook, M. L. H., Sayigh, L. S., Blum, J. E., and Wells, R. S. (2004). identified fine scale geographic variation between two “Signature-whistle production in undisturbed free-ranging bottlenose regions in the SWIO. Our results have highlighted key dif- dolphins (Tursiops truncatus),” Proc. R. Soc. London, Ser. B 271, ferences between the whistle contours of T. aduncus and 1043–1049. T. truncatus. Further research is necessary to understand the Cranford, T. W., Amundin, M., and Norris, K. S. (1996). “Functional mor- phology and homology in the odontocete nasal complex: implications for function of whistle contours in the communication system of sound generation,” J. Morphol. 228, 223–285. T. aduncus and investigate whether this species uses signa- Dıaz Lopez, B. (2011). “Whistle characteristics in free-ranging bottlenose ture whistles in the same way as T. truncatus. dolphins (Tursiops truncatus) in the Mediterranean Sea: influence of behaviour,” Mamm. Biol. 76, 180–189. dos Santos, M. E., Louro, S., Couchinho, M., and Brito, C. (2005). “Whistles ACKNOWLEDGMENTS of bottlenose dolphins (Tursiops truncatus) in the Sado Estuary, Portugal: This work was supported by a NERC studentship, a Uni- characteristics, production rates and long-term contour stability,” Aquat. Mamm. 31, 453–462. versity of St. Andrews Russell Trust Award to T.G., a Royal Esch, H. C., Sayigh, L. S., and Wells, R. S. 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4040 J. Acoust. Soc. Am., Vol. 132, No. 6, December 2012 Gridley et al.: Whistles of Indo-Pacific bottlenose dolphins Author's complimentary copy