Whistle variation in Mediterranean common bottlenose dolphin: The role of geographical,anthropogenic, social,and behavioral factors

The studies on the variation of acoustic communication in different species have provided insight that genetics, geographic isolation, and adaptation to ecological and social conditions play important roles in the variability of acoustic signals. The dolphin whistles are communication signals that can vary significantly among and within populations. Although it is known that they are influenced by different environmental and social variables, the factors influencing the variation between populations have received scant attention. In the present study, we investigated the factors associated with the acoustic variability in the whistles of common bottlenose dolphin (Tursiops truncatus), inhabiting two Mediterranean areas (Sardinia and Croatia). We explored which factors, among (a) geographical isolation of populations, (b) different environments in terms of noise and boat presence, and (c) social factors (including group size, behavior, and presence of calves), were associated with whistle characteristics. We first applied a principal component analysis to reduce the number of collinear whistle frequency and temporal characteristics and then generalized linear mixed models on the first two principal components. The study revealed that both geographic distance/isolation and local environment are associated with whistle variations between localities. The prominent differences in the acoustic environments between the two areas, which contributed to the acoustic variability in the first principal component (PC1), were found. The calf's presence and foraging and social behavior were also found to be associated with dolphin whistle variation. The second principal component (PC2) was associated only with locality and group size, showing that longer and more complex tonal sound may facilitate individual recognition and cohesion in social groups. Thus, both social and behavioral context influenced significantly the structure of whistles, and they should be considered when investigating acoustic variability among distant dolphin populations to avoid confounding factors.     

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.     

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.     

Bottlenose dolphins that forage with artisanal fishermen whistle differently

Acoustic communication is a taxonomically widespread phenomenon, crucial for social animals. We evaluate social sounds from bottlenose dolphins (Tursiops truncatus) of Laguna, southern Brazil, whose social structure is organized around a cooperative foraging tactic with artisanal fishermen. This tactic involves stereotyped and coordinated behaviour by dolphins and fishermen and is performed by a subset of the dolphin population, splitting it into two distinct social communities. We compared the acoustic parameters and type of whistles emitted by dolphins of the “non‐cooperative” and “cooperative” communities, both during their interactions with fishermen and in times where dolphins were engaged in other types of foraging. Our findings show how dolphins’ social sounds differ between foraging tactics and social communities. The frequencies of six whistle types (ascending, descending, concave, convex, multiple, flat) were significantly dependent on tactics and communities. Ascending whistles were more common than expected during foraging without fishermen, and among dolphins of the non‐cooperative community. Whistle acoustic parameters (duration, number of inclination changes and inflection points, and initial, final, maximum, minimum frequencies) also varied between social communities. In general, whistles emitted by cooperative dolphins, mainly when not interacting with fishermen, tended to be shorter, had higher frequency and more inflections than those emitted by non‐cooperative dolphins. These results suggest that different whistles may convey specific information among dolphins related to foraging, which we hypothesize promote social cohesion among members of the same social community. These differences in acoustic repertoires add a new dimension of complexity to this unique human–animal interaction.     

Whistle discrimination and categorization by the Atlantic bottlenose dolphin (Tursiops truncatus): a review of the signature whistle framework and a perceptual test

Dolphin whistles vary by frequency contour, changes in frequency over time. Individual dolphins may broadcast their identities via uniquely contoured whistles, "signature whistles." A recent debate concerning categorization of these whistles has highlighted the on-going need for perceptual studies of whistles by dolphins. This article reviews research on dolphin whistles as well as presenting a study in which a captive, female, adult bottlenose dolphin performed a conditional matching task in which whistles produced by six wild dolphins in Sarasota Bay were each paired with surrogate producers, specific objects/places. The dolphin subject also categorized unfamiliar exemplars produced by the whistlers represented by the original stimuli. The dolphin successfully discriminated among the group of whistles, associated them with surrogate producers, grouped new exemplars of the same dolphin's whistle together when the contour was intact, and discriminated among same-contour whistles produced by the same dolphin. Whistle sequences that included partial contours were not categorized with the original whistlers. Categorization appeared to be based on contour rather than specific acoustic parameters or voice cues. These findings are consistent with the perceptual tenets associated with the signature whistle framework which suggests that dolphins use individualized whistle contours for identification of known conspecifics.     

Differences in acoustic signals from Delphinids in the western North Atlantic and northern Gulf of Mexico

Whistle characteristics were quantitatively compared between both geographically separated and neighboring populations of Atlantic spotted dolphins (Stenella frontalis), bottlenose dolphins (Tursiops truncatus), and pilot whales (Globicephala spp.) in U.S. waters to evaluate if intraspecific acoustic differences exist between groups. We compared nine whistle characteristics between continental shelf and offshore Atlantic spotted dolphins in the western North Atlantic and between northern Gulf of Mexico and western North Atlantic bottlenose dolphins and pilot whales using discriminant analysis. Offshore Atlantic spotted dolphin whistles were significantly different (Hotelling's T², P= 0.0003) from continental shelf whistles in high frequency, bandwidth, duration, number of steps, and number of inflection points. Atlantic bottlenose dolphin whistles were significantly different (Hotelling's T², P < 0.0001) from those in the Gulf of Mexico in duration, number of steps, and number of inflection points. There was no significant difference between pilot whale whistles in the two basins. The whistle differences indicate acoustic divergence between groups in different areas that may arise from geographic isolation or habitat separation between neighboring but genetically distinct populations of dolphins. This study supports the premise that acoustic differences can be a tool to evaluate the ecological separation between marine mammal groups in field studies.     

Vertical auditory acuity of the bottlenose dolphin

The accuracy in locating underwater sounds in the vertical median plane was determined for the Black Sea bottlenose dolphin Tursiops truncatus trained by operant conditioning with food reinforcement. The minimal perceived angles for 1-s tone signals were 2.5° at 5 or 20 kHz and 2.0° at 120 kHz; for 1-s trains of clicks centered at 120 kHz the acuity was still better, ～1.5°. Dolphins may locate different sounds using different yet equally efficient mechanisms, and they are the best in analyzing the acoustic space among marine mammals studied.     

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.     

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.     

Sound reception in marine mammals depending on sound parameters and conduction pathways

The interaction of complex sounds with the body tissues of Black Sea dolphin (Tursiops truncatus) was studied by the method of instrumental conditioned reflexes with food reinforcement. The thresholds of detecting underwater acoustic signals of different frequencies for dolphin and northern fur seal (Callorhinus ursinus) were measured as a function of pulse duration under conditions of full and partial (head above water) submergence of animals into water. It was found that sound conduction through dolphin tissues was more effective than that in a northern fur seal in a wide frequency range. Presumably, the process of sound propagation in dolphin is accompanied by changes in the amplitude-frequency structure of broad-band sounds. The temporal summation in dolphin hearing was observed at all frequencies under conditions of full and partial submergence, whereas in northern fur seal it was nearly absent at a frequency of 5 kHz under the conditions of head lifting above water.     

A Permanent Automated Real-Time Passive Acoustic Monitoring System for Bottlenose Dolphin Conservation in the Mediterranean Sea

Within the framework of the EU Life+ project named LIFE09 NAT/IT/000190 ARION, a permanent automated real-time passive acoustic monitoring system for the improvement of the conservation status of the transient and resident population of bottlenose dolphin (Tursiops truncatus) has been implemented and installed in the Portofino Marine Protected Area (MPA), Ligurian Sea. The system is able to detect the simultaneous presence of dolphins and boats in the area and to give their position in real time. This information is used to prevent collisions by diffusing warning messages to all the categories involved (tourists, professional fishermen and so on). The system consists of two gps-synchronized acoustic units, based on a particular type of marine buoy (elastic beacon), deployed about 1 km off the Portofino headland. Each one is equipped with a four-hydrophone array and an onboard acquisition system which can record the typical social communication whistles emitted by the dolphins and the sound emitted by boat engines. Signals are pre-filtered, digitized and then broadcast to the ground station via wi-fi. The raw data are elaborated to get the direction of the acoustic target to each unit, and hence the position of dolphins and boats in real time by triangulation.     

LOW FREQUENCY NARROW-BAND SOUNDS PRODUCED BY BOTTLENOSE DOLPHINS

We present a new sound type recorded from bottlenose dolphins, Tursiops truncatus , in eastern Australian waters: low-frequency, narrow-band (LFN) harmonic sounds (defined as less than 2 kHz). Most of these sounds were of frequencies less than 1 kHz and were recorded commonly from socializing dolphins. These sounds differ significantly from narrow-band whistles, which are higher in frequency and longer in duration. The absence of these sounds in most studies of the acoustic behavior of bottlenose dolphins may reflect geographic differences in repertoires or result from insufficient sampling. Alternatively, these sounds may have been ignored where the focus of research was on other sound types.     

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.     

Dolphins Adjust Species-Specific Frequency Parameters to Compensate for Increasing Background Noise

An increase in ocean noise levels could interfere with acoustic communication of marine mammals. In this study we explored the effects of anthropogenic and natural noise on the acoustic properties of a dolphin communication signal, the whistle. A towed array with four elements was used to record environmental background noise and whistles of short-beaked common-, Atlantic spotted- and striped-dolphins in the Canaries archipelago. Four frequency parameters were measured from each whistle, while Sound Pressure Levels (SPL) of the background noise were measured at the central frequencies of seven one-third octave bands, from 5 to 20 kHz. Results show that dolphins increase the whistles’ frequency parameters with lower variability in the presence of anthropogenic noise, and increase the end frequency of their whistles when confronted with increasing natural noise. This study provides the first evidence that the synergy among SPLs has a role in shaping the whistles'' structure of these three species, with respect to both natural and anthropogenic noise.     

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.     

Vocalizations and Behaviour of Pacific Humpback Dolphins Sousa chinensis

Very little is known about the acoustic repertoire of the Pacific humpback dolphin Sousa chinensis . This study, off eastern Australia, used concurrent observations of surface behaviour and acoustic recordings to gain an insight into the behavioural significance of humpback dolphin vocalizations. Humpback dolphins exhibit five different vocalization categories: broad band clicks; barks; quacks; grunts; and whistles. Broad band clicks were high in frequency (8 kHz to > 22 kHz), were directly related to foraging behaviour and may play a role in social behaviour. Barks and quacks were burst pulse sounds (frequency: 0.6 kHz to > 22 kHz, duration: 0.1–8 s) and were associated with both foraging and social behaviour. The grunt vocalization is a low frequency narrow band sound (frequency 0.5–2.6 kHz, duration 0.06–2 s) and was only heard during socializing. There were 17 different types of whistles, ranging widely in frequency (0.9–22 kHz) and vocal structure (n=329). The predominant whistle types used by the groups were type 1 (46%) and type 2 (17%). Most whistles were heard during both socializing and foraging. The number of whistles recorded in a group increased significantly as the number of mother–calf pairs increased, suggesting that whistles may be used as contact calls. Few vocalizations were heard during either travelling or milling behaviours. Broad band clicks, barks and whistle type 1 were the only vocalizations recorded during either travelling or milling.     

Individual patterns of tonal (whistling) signals of bottlenose dolphins (Tursiops truncates) kept in relative isolation

The results of study of the subaqueous acoustic signaling of bottlenose dolphins (Tursiopsis truncatus) in a dolphinarium are shown. Individual patterns of whistling signals of four individuals were described and analyzed. To determine which animal produced the sound, the method of ??relative isolation?? was used. It was found that the pattern included whistles specific for a particular individual (??signature whistles??). The percentage of these whistles in the patterns varied considerably among individuals. The signatures had variable frequency and duration. The phenomenon of ??imitation?? was typical for animals at higher positions in the hierarchy: generating ??signatures?? specific for other individuals. Besides the signatures, variable signals and whistles with simple frequency contours were found in the patterns.     

Frequency discrimination by the bottle-nosed dolphin and the Northern fur seal depending on sound parameters and sound conduction pathways

Underwater differential frequency hearing thresholds in the Black Sea bottle-nosed dolphin (Tursiops truncatus p.) and the northern fur seal (Callorhinus ursinus) were measured depending on signal frequency and sound conduction pathways. The measurements were performed by the method of instrumental conditioned reflexes with food reinforcement under conditions of full and partial (with heads out of water at sound conduction through body tissues) submergence of animals into water. It was shown that in a frequency range of 5-100 kHz, underwater differential frequency hearing thresholds of the bottle-nosed dolphin changed from 0.46-0.60% to 0.21-0.34% and depended little on sound conduction pathways. The minimum underwater differential frequency hearing thresholds of the northern fur seal corresponded to the frequencies of maximum hearing sensitivity, changed from 1.7% to 1-2.3% in a frequency range of 1-20 kHz, sharply increased at the edges of the frequency hearing perception range, and depended little (in a range of 5-40 kHz) on sound conduction pathways. Thus, underwater sounds propagating through the body tissues of dolphin and fur seal reach the inner ear.     

Day and night sounds of the Guiana dolphin, <Emphasis Type="Italic">Sotalia guianensis</Emphasis> (Cetacea: Delphinidae) in southeastern Brazil

Many cetaceans are known to be acoustically active at night. However, for most dolphin species, there is little information about their nocturnal acoustic activities. To study the acoustic repertoire of Sotalia guianensis, diurnal and nocturnal sounds (whistles, burst pulses, low-frequency narrowband (LFN) sounds, and clicks) were identified in the Cananéia estuary (25° 01′ S–25° 13′ S/47° 52′ W–48° 06′ W), south of the state of São Paulo, southeastern Brazil, during April, June, and November of 2012. The emission rate of these sounds was compared between daytime and nighttime using the chi-squared statistical test. The mean values of the acoustic parameters of whistles, burst pulses, LFN sounds, and clicks were compared using the t test. Whistles, burst pulses, and LFN sounds were more frequent at night, as these individuals require greater acoustic communication in the absence of light, mainly for social communication. Echolocation emission rates were similar in both day and nighttime. Dolphin sound structure also varied throughout the day, with dolphins emitting lower-frequency sounds at night. Low-frequency sounds, with longer wavelengths, provide many advantages for dolphins active at night because such sounds propagate greater distances. This study demonstrates that the sounds produced by S. guianensis are dependent on the time of day, with social communication sounds being more influenced by the presence of light.     

Sonar-induced temporary hearing loss in dolphins

There is increasing concern that human-produced ocean noise is adversely affecting marine mammals, as several recent cetacean mass strandings may have been caused by animals'' interactions with naval ‘mid-frequency’ sonar. However, it has yet to be empirically demonstrated how sonar could induce these strandings or cause physiological effects. In controlled experimental studies, we show that mid-frequency sonar can induce temporary hearing loss in a bottlenose dolphin (Tursiops truncatus). Mild-behavioural alterations were also associated with the exposures. The auditory effects were induced only by repeated exposures to intense sonar pings with total sound exposure levels of 214 dB re: 1 μPa² s. Data support an increasing energy model to predict temporary noise-induced hearing loss and indicate that odontocete noise exposure effects bear trends similar to terrestrial mammals. Thus, sonar can induce physiological and behavioural effects in at least one species of odontocete; however, exposures must be of prolonged, high sound exposures levels to generate these effects.