Quantitative Comparison of Whistle Repertoires from Captive Adult Bottlenose Dolphins (Delphinidae,Tursiops truncatus): a Re-evaluation of the Signature Whistle Hypothesis

The prevailing view among researchers of dolphin communication is that bottlenose dolphins possess an individualized whistle contour; known as the ‘signature whistle’, it accounts for 74–95 % of a dolphin's whistle repertoire and functions to signal the individual identity of the whistler. This study used a new quantitative technique, termed the contour similarity technique (CS technique), and reports on the quantitative comparison of whistles from the individuals of three different social groups of bottlenose dolphins in socially interactive contexts. Results suggest that captive adult dolphins share several different whistle types including one predominant whistle type shared by all individuals across three different social groups. These analyses suggest a different interpretation of the dolphin whistle repertoire than has previously been proposed by proponents of the signature whistle hypothesis. In addition, results from our study support the results of early studies, published before the advent of the signature whistle hypothesis, in which investigators reported a large whistle repertoire within socially interactive captive and free-ranging groups and a predominant whistle type similar to that found in our study. Our results, combined with the results from earlier studies of dolphin vocal behaviour, suggest that the signature whistle hypothesis is incomplete and that dolphin whistle repertoires need to be analysed with respect to behavioural context and social relationships. In addition, these results suggest that contour discrimination and other acoustic features of whistles need to be tested in perception and categorization experiments.     

A New Quantitative Technique for Categorizing Whistles Using Simulated Signals and Whistles from Captive Bottlenose Dolphins (Delphinidae,Tursiops truncatus)

A widespread problem in the study of animal vocalizations is evaluating the acoustic similarity of signals both between individuals of a social group and between social groups. This problem becomes especially salient when classifying the narrow-band frequency-modulated signals, such as whistles, found in many avian and mammalian species. Whistles are usually characterized by their relative change in frequency over time, known as whistle ‘contour’. Measuring such a characteristic is difficult as it is not a single measurement, such as the mean frequency or duration of a signal, but several associated measurements of frequency across time. This paper reports on a new quantitative technique for determining whistle types based on whistle contour similarity and an application of this technique to the whistles of bottlenose dolphins to demonstrate its utility. This ‘contour similarity’ technique (CS technique) uses cluster analysis to group the correlation coefficients of frequency measurements from a data set of signals. To demonstrate the efficacy of this CS technique, three data sets were analysed, two using computer-generated signals and a third using adult bottlenose dolphin whistles, to (1) examine the efficacy of correlation coefficients for grouping signals by their similarity in whistle contour and (2) determine the viability of this technique for categorizing bottlenose dolphin whistles. Measured actual frequencies and correlation matrices from the four simulated signal types and a correlation matrix from the whistles of five captive adult bottlenose dolphins were each subjected to K-means cluster analysis and the resulting signal types were evaluated. Results indicated that the technique grouped actual frequencies according to the amount of shared actual frequencies and grouped correlation coefficients successfully according to signal contour. This result endured even if contours differed in overall duration or actual frequency or were expanded or compressed with respect to frequency or time. The results suggest that this approach is a viable method for assigning whistle contours to categories in bottlenose dolphins or any other species with narrow-band, frequency-modulated signals.     

Dolphin whistles: a functional misnomer revealed by heliox breathing

Delphinids produce tonal whistles shaped by vocal learning for acoustic communication. Unlike terrestrial mammals, delphinid sound production is driven by pressurized air within a complex nasal system. It is unclear how fundamental whistle contours can be maintained across a large range of hydrostatic pressures and air sac volumes. Two opposing hypotheses propose that tonal sounds arise either from tissue vibrations or through actual whistle production from vortices stabilized by resonating nasal air volumes. Here, we use a trained bottlenose dolphin whistling in air and in heliox to test these hypotheses. The fundamental frequency contours of stereotyped whistles were unaffected by the higher sound speed in heliox. Therefore, the term whistle is a functional misnomer as dolphins actually do not whistle, but form the fundamental frequency contour of their tonal calls by pneumatically induced tissue vibrations analogous to the operation of vocal folds in terrestrial mammals and the syrinx in birds. This form of tonal sound production by nasal tissue vibrations has probably evolved in delphinids to enable impedance matching to the water, and to maintain tonal signature contours across changes in hydrostatic pressures, air density and relative nasal air volumes during dives.     

Identifying signature whistles from recordings of groups of unrestrained bottlenose dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) have individually distinctive signature whistles. Each individual dolphin develops its own unique frequency modulation pattern and uses it to broadcast its identity. However, underwater sound localization is challenging, and researchers have had difficulties identifying signature whistles. The traditional method to identify them involved isolating individuals. In this context, the signature whistle is the most commonly produced whistle type of an animal. However, most studies on wild dolphins cannot isolate animals. We present a novel method, SIGnature IDentification (SIGID), that can identify signature whistles in recordings of groups of dolphins recorded via a single hydrophone. We found that signature whistles tend to be delivered in bouts with whistles of the same type occurring within 1–10 s of each other. Nonsignature whistles occur with longer or shorter interwhistle intervals, and this distinction can be used to identify signature whistles in a recording. We tested this method on recordings from wild and captive bottlenose dolphins and show thresholds needed to identify signature whistles reliably. SIGID will facilitate the study of signature whistle use in the wild, signature whistle diversity between different populations, and potentially allow signature whistles to be used in mark‐recapture studies.     

Bottlenose dolphins exchange signature whistles when meeting at sea

The bottlenose dolphin, Tursiops truncatus, is one of very few animals that, through vocal learning, can invent novel acoustic signals and copy whistles of conspecifics. Furthermore, receivers can extract identity information from the invented part of whistles. In captivity, dolphins use such signature whistles while separated from the rest of their group. However, little is known about how they use them at sea. If signature whistles are the main vehicle to transmit identity information, then dolphins should exchange these whistles in contexts where groups or individuals join. We used passive acoustic localization during focal boat follows to observe signature whistle use in the wild. We found that stereotypic whistle exchanges occurred primarily when groups of dolphins met and joined at sea. A sequence analysis verified that most of the whistles used during joins were signature whistles. Whistle matching or copying was not observed in any of the joins. The data show that signature whistle exchanges are a significant part of a greeting sequence that allows dolphins to identify conspecifics when encountering them in the wild.     

Biphonal calls in Atlantic spotted dolphins (Stenella frontalis): bitonal and burst-pulse whistles

Biphonation, the simultaneous production of two sounds by a single animal, is found in the vocalizations of a range of mammalian species. Its prevalence suggests it plays an important role in acoustic communication. Concurrent vocal and behavioural recordings were made of Atlantic spotted dolphins (Stenella frontalis) off Bimini, The Bahamas. The occurrence of two types of biphonal signals is reported: burst-pulse whistles with combined tonal and burst-pulse elements, and bitonal whistles. Biphonal whistles are rarely described in reports of dolphin acoustic repertoires, but were common in these dolphins: of all whistles analysed (n = 1211), 26.84% were burst-pulse whistles and 4.71% were bitonal whistles. A subset of whistles (n = 397) were attributed to dolphins of specific age classes, and used to compare prevalence of biphonation across age. Biphonation occurred in 61.54% of sexually mature and 48.32% of sexually immature dolphins’ whistles. Sexually immature dolphins emitted more burst-pulse whistles than older dolphins: 44.13% of sexually immature dolphins’ whistles were burst-pulse whistles, while 15.38% of adult whistles were burst-pulse whistles. Bitonal whistle production was more prevalent in sexually mature dolphins: 41.03% of adult whistles were bitonal, while only 4.19% of sexually immature dolphins’ whistles were bitonal. The prevalence of a biphonal component in specific repeated, stereotyped whistle contours suggests that these acoustic features could be important components of contact calls, or signature whistles. The biphonal components of spotted dolphin whistles may serve to convey additional information as to identity, age or other factors to conspecifics.     

Recognition of Frequency Modulated Whistle-Like Sounds by a Bottlenose Dolphin (Tursiops truncatus) and Humans with Transformations in Amplitude,Duration and Frequency

Bottlenose dolphins (Tursiops truncatus) use the frequency contour of whistles produced by conspecifics for individual recognition. Here we tested a bottlenose dolphin’s (Tursiops truncatus) ability to recognize frequency modulated whistle-like sounds using a three alternative matching-to-sample paradigm. The dolphin was first trained to select a specific object (object A) in response to a specific sound (sound A) for a total of three object-sound associations. The sounds were then transformed by amplitude, duration, or frequency transposition while still preserving the frequency contour of each sound. For comparison purposes, 30 human participants completed an identical task with the same sounds, objects, and training procedure. The dolphin’s ability to correctly match objects to sounds was robust to changes in amplitude with only a minor decrement in performance for short durations. The dolphin failed to recognize sounds that were frequency transposed by plus or minus ½ octaves. Human participants demonstrated robust recognition with all acoustic transformations. The results indicate that this dolphin’s acoustic recognition of whistle-like sounds was constrained by absolute pitch. Unlike human speech, which varies considerably in average frequency, signature whistles are relatively stable in frequency, which may have selected for a whistle recognition system invariant to frequency transposition.     

Assessing spatial patterns and density of a dolphin population through signature whistles

Some dolphin species produce signature whistles, which may allow the identification of individual dolphins using passive acoustic monitoring (PAM). Identifying individuals by their sounds may enhance the opportunities for monitoring and addressing biological and ecological questions about these species. Here, we explored the potential of signature whistles to investigate ecological aspects of a resident bottlenose dolphin population. Using a limited data set, with few individuals recognized by signature whistles, combined with spatial capture-recapture (SCR) methods, we investigated how effective such approach is describing spatial use patterns and estimating density for this population. The data were collected using 4–6 stationary bottom-moored recorders. Since only eight signature whistles were identified, our density estimate may represent a subset of the entire population. However, even with only a few signature whistles identified, our results confirmed the center of the core area used by these dolphins as the area with the highest encounter probability. In addition, our results provided evidence that these dolphins have the same spatial use pattern at night as during the day. This study shows that SCR analysis of signature whistle data can improve our ecological knowledge and understanding of dolphin populations.     

Postpartum whistle production in bottlenose dolphins

Despite much research on bottlenose dolphin signature whistles, few have investigated the role of maternal whistles in early calf development. We investigated maternal whistle use in the first weeks postpartum for captive dolphins. The overall whistling rate increased by a factor of ten when the calves were born and then decreased again in the third week of the one surviving calf. Adult whistles were distinguished from calf whistles based on the extent of frequency modulation and were further classified into signature and non-signature whistles by comparison to a dictionary of known whistles. The average rate of maternal signature whistle production increased significantly from 0.02 whistles per dolphin-minute before the calves were born to 0.2 and 0.3 whistles in weeks 1 and 2, decreasing again to 0.06 in week 3 for the mother of the surviving calf. Percent maternal signature whistles changed similarly. Signature whistle production by non-mothers did not change when the calves were born. A likely function of this increase in maternal signature whistle production is that it enables the calf to learn to identify the mother in the first weeks of life.     

DEVELOPMENT AND SOCIAL FUNCTIONS OF SIGNATURE WHISTLES IN BOTTLENOSE DOLPHINS TURSIOPS TRUNCATUS

ABSTRACT

Bottlenose dolphins Tursiops truncatus produce individually distinctive signature whistles. Dolphins recognize the signature whistles of animals with which they share a social bond. Signature whistles develop within the first few months of life and are stable for a lifetime. Vocal learning appears to play a role in the development of signature whistles in bottlenose dolphins. The signature whistles of most female dolphins and about half of male dolphins differ from those of their mothers. Some dolphin calves born in captivity develop a signature whistle that matches either man-made whistles or those of an unrelated dolphin. Dolphins retain the ability as adults to imitate the whistles of animals with which they share strong individual-specific social relationships, bonds which may change throughout their lifetime. The exceptional imitative abilities of dolphin infants and the retention of this ability in adults may be related to the maintenance of changing individual specific social relationships. Individual recognition by the voice may differ in marine vs terrestrial mammals. Diving marine mammals may not be able to rely upon involuntary voice cues for individual recognition, but rather may require vocal learning to maintain a stable signature as their vocal tract changes shape with increasing pressure during a dive.     

What’s occurring? Ultrasonic signature whistle use in Welsh bottlenose dolphins (Tursiops truncatus)

Animal communication signals are diverse. The types of sounds that animals produce, and the way that information is encoded in those sounds, not only varies between species but can also vary geographically within a species. Therefore, an understanding of the vocal repertoire at the population level is important for providing insight into regional differences in vocal communication signals. One species whose vocal repertoire has received considerable attention is the bottlenose dolphin. This species is well known for its use of individually distinctive identity signals, known as signature whistles. Bottlenose dolphins use their signature whistles to broadcast their identity and to maintain contact with social companions. Signature whistles are not innate, but are learnt signals that develop within the first few months of an animal’s life. It is therefore unsurprising that studies which have characterized signature whistles in wild populations of bottlenose dolphins have provided evidence of geographic variation in signature whistle structure. Here, we describe the occurrence of signature whistles in a previously unexplored wild population of bottlenose dolphins in Cardigan Bay, Wales. We present the first occurrence of a signature whistle with an ultrasonic fundamental frequency component (>30 kHz), a frequency band that was not thought to be utilized by this species for whistle communication. We also describe the occurrence of an ultrasonic non-signature whistle. Our findings highlight the importance of conducting regional studies in order to fully quantify a species’ vocal repertoire, and call into question the efficacy of those studies that use restricted sampling rates.     

Signature whistles in wild bottlenose dolphins: long-term stability and emission rates

Whistles are key elements in the acoustic repertoire of bottlenose dolphins. In this species, the frequency contours of whistles are used as individual signatures. Assessing the long-lasting stability of such stereotyped signals, and the abundant production of non-stereotyped whistles in the wild, is relevant to a more complete understanding of their biological function. Additionally, studying the effects of group size and activity patterns on whistle emission rate may provide insights into the use of these calls. In this study, we document the decades-long occurrence of whistles with stereotyped frequency contours in a population of wild bottlenose dolphins, resident in the region of the Sado estuary, Portugal. Confirmed stereotypy throughout more than 20 years, and positive identification using the signature identification (SIGID) criteria, suggests that the identified stereotyped whistles are in fact signature whistles. The potential roles of non-stereotyped whistles, which represent 68 % of all whistles recorded, are still unclear and should be further investigated. Emission rates were significantly higher during food-related events. Finally, our data show a comparatively high overall whistle production for this population, and no positive correlation between group size and emission rates, suggesting social or environmental restriction mechanisms in vocal production.     

Signature whistles in free‐ranging populations of Indo‐Pacific bottlenose dolphins,Tursiops aduncus

Common bottlenose dolphins (Tursiops truncatus) use individually distinctive signature whistles which are highly stereotyped and function as contact calls. Here we investigate whether Indo‐Pacific bottlenose dolphins (T. aduncus) use signature whistles. The frequency trace of whistle contours recorded from three genetically distinct free‐ranging populations was extracted and sorted into whistle types of similar shape using automated categorization. A signature whistle identification method based on the temporal patterns in signature whistle sequences of T. truncatus was used to identify signature whistle types (SWTs). We then compared the degree of variability in SWTs for several whistle parameters to determine which parameters are likely to encode identity information. Additional recordings from two temporarily isolated T. aduncus made during natural entrapment events in 2008 and 2009 were analyzed for the occurrence of SWTs. All populations were found to produce SWTs; 34 SWTs were identified from recordings of free‐ranging T. aduncus and one SWT was prevalent in each recording of the two temporarily isolated individuals. Of the parameters considered, mean frequency and maximum frequency were the least variable and therefore most likely to reflect identity information encoded in frequency modulation patterns. Our results suggest that signature whistles are commonly used by T. aduncus.     

Pitfalls in the categorization of behaviour: a comparison of dolphin whistle classification methods

The categorization of behaviour patterns into separate classes is crucial to the study of animal behaviour. Traditionally researchers have classified behaviour patterns through careful observation by eye. Recently this method has been increasingly replaced by computer methods. While the definition and fine scale analysis that can be achieved with computers is desirable, only a few studies have actually looked at how these methods perform in comparison with human observation. I compared the classification of bottlenose dolphin, Tursiops truncatus, whistles by human observers with the performance of three computer methods: (1) a method developed by McCowan (1995, Ethology, 100, 177-193); (2) a comparison of cross-correlation coefficients using hierarchical cluster analysis; and (3) a comparison of average difference in frequency along two whistle contours also using hierarchical cluster analysis. The whistle sample consisted of 104 randomly chosen whistles from a group of four captive bottlenose dolphins recorded both during periods when one was separate from the rest of the group and while they all swam in the same pool. The sample contained five individual-specific signature whistles and several nonsignature whistles. Five human observers, without knowledge of the recording context, were more likely than the computer methods to identify signature whistles that were used only while an animal was isolated from the rest of the group. I discuss the limitations of methods commonly used for pattern recognition in communication studies. The discrepancies between methods show how crucial it is to obtain an external validation of the behaviour classes used in studies of animal behaviour. Copyright 1999 The Association for the Study of Animal Behaviour.     

Identification and Characteristics of Signature Whistles in Wild Bottlenose Dolphins (Tursiops truncatus) from Namibia

A signature whistle type is a learned, individually distinctive whistle type in a dolphin''s acoustic repertoire that broadcasts the identity of the whistle owner. The acquisition and use of signature whistles indicates complex cognitive functioning that requires wider investigation in wild dolphin populations. Here we identify signature whistle types from a population of approximately 100 wild common bottlenose dolphins (Tursiops truncatus) inhabiting Walvis Bay, and describe signature whistle occurrence, acoustic parameters and temporal production. A catalogue of 43 repeatedly emitted whistle types (REWTs) was generated by analysing 79 hrs of acoustic recordings. From this, 28 signature whistle types were identified using a method based on the temporal patterns in whistle sequences. A visual classification task conducted by 5 naïve judges showed high levels of agreement in classification of whistles (Fleiss-Kappa statistic, κ = 0.848, Z = 55.3, P<0.001) and supported our categorisation. Signature whistle structure remained stable over time and location, with most types (82%) recorded in 2 or more years, and 4 identified at Walvis Bay and a second field site approximately 450 km away. Whistle acoustic parameters were consistent with those of signature whistles documented in Sarasota Bay (Florida, USA). We provide evidence of possible two-voice signature whistle production by a common bottlenose dolphin. Although signature whistle types have potential use as a marker for studying individual habitat use, we only identified approximately 28% of those from the Walvis Bay population, despite considerable recording effort. We found that signature whistle type diversity was higher in larger dolphin groups and groups with calves present. This is the first study describing signature whistles in a wild free-ranging T. truncatus population inhabiting African waters and it provides a baseline on which more in depth behavioural studies can be based.     

Whistling in a noisy ocean: bottlenose dolphins adjust whistle frequencies in response to real-time ambient noise levels

Common bottlenose dolphins (Tursiops truncatus) use complex acoustic behaviours for communication, group cohesion and foraging. Ambient noise from natural and anthropogenic sources has implications for the acoustic behaviour of dolphins, and research shows that average ambient noise levels alter dolphin acoustic behaviour. However, when background noise levels are highly variable, the relationships between noise and acoustic behaviour over short time periods are likely important. This study investigates whether bottlenose dolphins altered the temporal and spectral qualities of their whistles in relation to the ambient noise present at the time the whistles were produced. Dolphin groups were recorded in Tampa Bay (western Florida) between 2008 and 2015. Six whistle parameters were analysed in spectrogram software (minimum frequency, maximum frequency, bandwidth, peak frequency, duration and number of inflection points) and ambient noise levels were calculated immediately prior to each whistle. Linear regression analysis indicated that the minimum, maximum and peak frequencies of whistles had significant positive relationships with the ambient noise levels present at the time of the whistles. These models suggested that for each 1 dB increase in ambient noise, minimum frequency increased by 121 Hz, maximum frequency increased by 108 Hz and peak frequency increased by between 122 and 144 Hz. As ambient noise is typically low frequency, this suggests that bottlenose dolphins increased whistle frequency in response to real-time noise levels to avoid masking. Future research to determine the fitness consequences of noise-induced changes in the communication behaviour of dolphins would be an important contribution to conservation efforts.     

Signature-whistle production in undisturbed free-ranging bottlenose dolphins (Tursiops truncatus)

Data from behavioural observations and acoustic recordings of free-ranging bottlenose dolphins (Tursiops truncatus) were analysed to determine whether signature whistles are produced by wild undisturbed dolphins, and how whistle production varies with activity and group size. The study animals were part of a resident community of bottlenose dolphins near Sarasota, Florida, USA. This community of dolphins provides a unique opportunity for the study of signature-whistle production, since most animals have been recorded during capture-release events since 1975. Three mother-calf pairs and their associates were recorded for a total of 141.25 h between May and August of 1994 and 1995. Whistles of undisturbed dolphins were compared with those recorded from the same individuals during capture-release events. Whistles were conservatively classified into one of four categories: signature, probable signature, upsweep or other. For statistical analyses, signature and probable signature whistles were combined into a 'signature' category; upsweep and other whistles were combined into a 'non-signature' category. Both 'signature' and 'non-signature' whistle frequencies significantly increased as group size increased. There were significant differences in whistle frequencies across activity types: both 'signature' and 'non-signature' whistles were most likely to occur during socializing and least likely to occur during travelling. There were no significant interactions between group size and activity type. Signature and probable signature whistles made up ca. 52% of all whistles produced by these free-ranging bottlenose dolphins.     

Communication in bottlenose dolphins: 50 years of signature whistle research

Bottlenose dolphins (Tursiops truncatus) produce individually distinctive signature whistles that broadcast the identity of the caller. Unlike voice cues that affect all calls of an animal, signature whistles are distinct whistle types carrying identity information in their frequency modulation pattern. Signature whistle development is influenced by vocal production learning. Animals use a whistle from their environment as a model, but modify it, and thus invent a novel signal. Dolphins also copy signature whistles of others, effectively addressing the whistle owner. This copying occurs at low rates and the resulting copies are recognizable as such by parameter variations in the copy. Captive dolphins can learn to associate novel whistles with objects and use these whistles to report on the presence or absence of the object. If applied to signature whistles, this ability would make the signature whistle a rare example of a learned referential signal in animals. Here, we review the history of signature whistle research, covering definitions, acoustic features, information content, contextual use, developmental aspects, and species comparisons with mammals and birds. We show how these signals stand out amongst recognition calls in animals and how they contribute to our understanding of complexity in animal communication.     

Differences in oscillatory whistles produced by spinner (Stenella longirostris) and pantropical spotted (Stenella attenuata) dolphins

Acoustic recordings of two closely related species, spinner dolphin (Stenella longirostris) and pantropical spotted dolphin (Stenella attenuata), were investigated from four different geographic locations: two in the Central Tropical Pacific, one in the Eastern Tropical Pacific and one in the Indian Ocean. The two delphinid species occur in tropical and warm temperate waters, with overlapping ranges. They produce very similar vocalizations, but at the same time their calls exhibit a certain degree of intraspecific variation among different geographic locations as has been observed in other delphinid species. Oscillatory whistles (whistles with at least two oscillations in their frequency contours) were identified and manually extracted from the recordings. Whistles with four or more maxima (oscillations) occurred only in spinner dolphins and they were present in all geographic regions investigated. In addition, the oscillatory whistles with two and three maxima were significantly more frequent in spinner than in spotted dolphins. The differences in oscillatory whistles for these two species seem to be consistent across study areas and therefore, could be used in addition to other whistle features to help distinguish between them.