Bottlenose dolphin mothers modify signature whistles in the presence of their own calves.

Human caregivers interacting with children typically modify their speech in ways that promote attention, bonding, and language acquisition. Although this "motherese," or child-directed communication (CDC), occurs in a variety of human cultures, evidence among nonhuman species is very rare. We looked for its occurrence in a nonhuman mammalian species with long-term mother-offspring bonds that is capable of vocal production learning, the bottlenose dolphin (Tursiops truncatus). Dolphin signature whistles provide a unique opportunity to test for CDC in nonhuman animals, because we are able to quantify changes in the same vocalizations produced in the presence or absence of calves. We analyzed recordings made during brief catch-and-release events of wild bottlenose dolphins in waters near Sarasota Bay, Florida, United States, and found that females produced signature whistles with significantly higher maximum frequencies and wider frequency ranges when they were recorded with their own dependent calves vs. not with them. These differences align with the higher fundamental frequencies and wider pitch ranges seen in human CDC. Our results provide evidence in a nonhuman mammal for changes in the same vocalizations when produced in the presence vs. absence of offspring, and thus strongly support convergent evolution of motherese, or CDC, in bottlenose dolphins. CDC may function to enhance attention, bonding, and vocal learning in dolphin calves, as it does in human children. Our data add to the growing body of evidence that dolphins provide a powerful animal model for studying the evolution of vocal learning and language.

The startle reflex in echolocating odontocetes: basic physiology and practical implications.

The acoustic startle reflex is an oligo-synaptic reflex arc elicited by rapid-onset sounds. Odontocetes evolved a range of specific auditory adaptations to aquatic hearing and echolocation, e.g. the ability to downregulate their auditory sensitivity when emitting clicks. However, it remains unclear whether these adaptations also led to changes of the startle reflex. We investigated reactions to startling sounds in two bottlenose dolphins (Tursiops truncatus) and one false killer whale (Pseudorca crassidens). Animals were exposed to 50 ms, 1/3 octave band noise pulses of varying levels at frequencies of 1, 10, 25 and 32 kHz while positioned in a hoop station. Startle responses were quantified by measuring rapid muscle contractions using a three-dimensional accelerometer attached to the dolphin. Startle magnitude increased exponentially with increasing received levels. Startle thresholds were frequency dependent and ranged from 131 dB at 32 kHz to 153 dB at 1 kHz (re. 1 µPa). Startle thresholds only exceeded masked auditory AEP thresholds of the animals by 47 dB but were ∼82 dB above published behavioural audiograms for these species. We also tested the effect of stimulus rise time on startle magnitude using a broadband noise pulse. Startle responses decreased with increasing rise times from 2 to 100 ms. Models suggested that rise times of 141-220 ms were necessary to completely mitigate startle responses. Our data showed that the startle reflex is conserved in odontocetes and follows similar principles as in terrestrial mammals. These principles should be considered when assessing and mitigating the effects of anthropogenic noise on marine mammals.

Bottlenose dolphin calves have multi-year elevations of plasma oxytocin compared to all other age classes.

Providing for infants nutritionally via lactation is one of the hallmarks of mammalian reproduction, and infants without motivated mothers providing for them are unlikely to survive. Mothers must maintain regular contact with infants both spatially and temporally while utilising their environment to forage, avoid threats and find shelter. However, mothers can only do this and maximise their reproductive success with some degree of co-operation from infants, despite their developing physical and cognitive capabilities. The neuropeptide hormone oxytocin (OT) triggers proximity-seeking behaviour and acts in a positive feedback loop across mother-infant bonds, stimulating appropriate pro-social behaviour across the pair. However, data on infant OT levels is lacking, and it is unclear how important infants are in maintaining mother-infant associations. The bottlenose dolphin (Tursiops truncatus) is a mammalian species that is fully physically mobile at birth and has multi-year, but individually variable, lactation periods. We investigated OT concentrations in mother-infant pairs of wild individuals compared to other age and reproductive classes. An ELISA to detect OT in dolphin plasma was successfully validated with extracted plasma. We highlight a statistical method for testing for parallelism that could be applied to other ELISA validation studies. OT concentrations were consistently elevated in calves up to at least 4 years of age with lactating mothers (12.1 ±â€¯0.9 pg/ml), while all mothers (4.5 ±â€¯0.4 pg/ml) had OT concentrations comparable to non-lactating individuals (5.9 ±â€¯0.5 pg/ml). Concentrations within infants were individually variable, and may reflect the strength of the bond with their mother. The OT system likely provides a physiological mechanism for motivating infants to perform behaviours that prevent long-term separation from their mothers during this crucial time in their life history. Elevated infant OT has also been linked to energetic and developmental advantages which may lead to greater survival rates. Environmental or anthropogenic disturbances to OT release can occur during bond formation or can disrupt the communication methods used to reinforce these bonds via OT elevation. Variation in OT expression in infants, and its behavioural and physiological consequences, may explain differences in reproductive success despite appropriate maternal behaviour expression.

Repeated downsweep vocalizations of the Araguaian river dolphin, Inia araguaiaensis.

Araguaian botos (Inia araguaiaensis) are known to produce pulsed as well as tonal sounds. This study documents the first evidence for repetitive sequences of downsweep whistles in botos that appear to be shared between individuals, and the context of their occurrence is investigated. Boat surveys were conducted along the Tocantins River located in the Eastern Amazon over a period of 42 days between 2012 and 2018. Eighty-two groups of Araguaian botos were observed, and 43 h of sound recordings were acquired. 632 downsweep whistles were recorded in 10 encounters. Four of these encounters contained downsweep bouts (21 bouts with ≥2 whistles) with short inter-call intervals (bout criterion 50 s) and up to 161 whistles. A statistical relationship was not found between downsweep occurrence and any of the contextual parameters that were investigated, including socializing, travelling, feeding, group size, presence of calves, and socio-sexual displays. The rarity of these signals makes them unlikely candidates for individual or group identification. It is more likely that they are associated with very specific contexts, such as nursing or mating, both of which were rarely observed in this study. Further studies are required to investigate context specificity and elucidate the function of these signals.

Signal-specific amplitude adjustment to noise in common bottlenose dolphins (Tursiops truncatus).

Anthropogenic underwater noise has increased over the past century, raising concern about the impact on cetaceans that rely on sound for communication, navigation and locating prey and predators. Many terrestrial animals increase the amplitude of their acoustic signals to partially compensate for the masking effect of noise (the Lombard response), but it has been suggested that cetaceans almost fully compensate with amplitude adjustments for increasing noise levels. Here, we used sound-recording DTAGs on pairs of free-ranging common bottlenose dolphins (Tursiops truncatus) to test (i) whether dolphins increase signal amplitude to compensate for increasing ambient noise and (ii) whether adjustments are identical for different signal types. We present evidence of a Lombard response in the range 0.1-0.3 dB per 1 dB increase in ambient noise, which is similar to that of terrestrial animals, but much lower than the response reported for other cetaceans. We found that signature whistles tended to be louder and with a lower degree of amplitude adjustment to noise compared with non-signature whistles, suggesting that signature whistles may be selected for higher output levels and may have a smaller scope for amplitude adjustment to noise. The consequence of the limited degree of vocal amplitude compensation is a loss of active space during periods of increased noise, with potential consequences for group cohesion, conspecific encounter rates and mate attraction.

Effects of impulsive noise on marine mammals: investigating range-dependent risk.

Concerns exist about the impacts of underwater noise on marine mammals. These include auditory damage, which is a significant risk for marine mammals exposed to impulsive sounds such as explosions, pile-driving, and seismic air guns. Currently, impact assessments use different risk criteria for impulsive and non-impulsive sounds (e.g., ships, drilling). However, as impulsive sounds dissipate through the environment, they potentially lose hazardous features (e.g., sudden onset) and become non-impulsive at some distance from the source. Despite management implications, a lack of data on range-dependent characteristics currently limits their inclusion in impact assessments. We address this using acoustic recordings of seismic air guns and pile-driving to quantify range dependency in impulsive characteristics using four criteria: (1) rise time < 25 ms; (2) quotient of peak pressure and pulse duration > 5,000 Pa/s; (3) duration < 1 s; (4) crest factor > 15 dB. We demonstrate that some characteristics changed markedly within ranges of ~10 km, and that the mean probability of exceeding criteria 1 and 2 was <0.5 at ranges >3.5 km. In contrast, the mean probability of exceeding criteria 3 remained >0.5 up to ~37.0 km, and the mean probability of exceeding criteria 4 remained <0.5 throughout the range. These results suggest that a proportion of the recorded signals should be defined as impulsive based on each of the criteria, and that some of the criteria change markedly as a result of propagation. However, the impulsive nature of a sound is likely to be a complex interaction of all these criteria, and many other unrelated parameters such as duty cycle, recovery periods, and sound levels will also strongly affect the risk of hearing damage. We recommend future auditory damage studies and impact assessments explicitly consider the ranges at which sounds may lose some of their potentially hazardous characteristics.

Selective reactions to different killer whale call categories in two delphinid species.

The risk of predation is often invoked as an important factor influencing the evolution of social organization in cetaceans, but little direct information is available about how these aquatic mammals respond to predators or other perceived threats. We used controlled playback experiments to examine the behavioral responses of short-finned pilot whales (Globicephala macrorhynchus) off Cape Hatteras, NC, USA, and Risso's dolphins (Grampus griseus) off the coast of Southern California, USA, to the calls of a potential predator, mammal-eating killer whales. We transmitted calls of mammal-eating killer whales, conspecifics and baleen whales to 10 pilot whales and four Risso's dolphins equipped with multi-sensor archival acoustic recording tags (DTAGs). Only playbacks of killer whale calls resulted in significant changes in tagged animal heading. The strong responses observed in both species occurred only following exposure to a subset of killer whale calls, all of which contained multiple non-linear properties. This finding suggests that these structural features of killer whale calls convey information about predatory risk to pilot whales and Risso's dolphins. The observed responses differed between the two species; pilot whales approached the sound source while Risso's dolphins fled following playbacks. These divergent responses likely reflect differences in anti-predator response mediated by the social structure of the two species.

What's in a voice? Dolphins do not use voice cues for individual recognition.

Most mammals can accomplish acoustic recognition of other individuals by means of "voice cues," whereby characteristics of the vocal tract render vocalizations of an individual uniquely identifiable. However, sound production in dolphins takes place in gas-filled nasal sacs that are affected by pressure changes, potentially resulting in a lack of reliable voice cues. It is well known that bottlenose dolphins learn to produce individually distinctive signature whistles for individual recognition, but it is not known whether they may also use voice cues. To investigate this question, we played back non-signature whistles to wild dolphins during brief capture-release events in Sarasota Bay, Florida. We hypothesized that non-signature whistles, which have varied contours that can be shared among individuals, would be recognizable to dolphins only if they contained voice cues. Following established methodology used in two previous sets of playback experiments, we found that dolphins did not respond differentially to non-signature whistles of close relatives versus known unrelated individuals. In contrast, our previous studies showed that in an identical context, dolphins reacted strongly to hearing the signature whistle or even a synthetic version of the signature whistle of a close relative. Thus, we conclude that dolphins likely do not use voice cues to identify individuals. The low reliability of voice cues and the need for individual recognition were likely strong selective forces in the evolution of vocal learning in dolphins.

Aerial low-frequency hearing in captive and free-ranging harbour seals (Phoca vitulina) measured using auditory brainstem responses.

The hearing sensitivity of 18 free-ranging and 10 captive harbour seals (Phoca vitulina) to aerial sounds was measured in the presence of typical environmental noise through auditory brainstem response measurements. A focus was put on the comparative hearing sensitivity at low frequencies. Low- and mid-frequency thresholds appeared to be elevated in both captive and free-ranging seals, but this is likely due to masking effects and limitations of the methodology used. The data also showed individual variability in hearing sensitivity with probable age-related hearing loss found in two old harbour seals. These results suggest that the acoustic sensitivity of free-ranging animals was not negatively affected by the soundscape they experienced in the wild.

Evidence suggests vocal production learning in a cross-fostered Risso's dolphin (Grampus griseus).

Vocal learning is a rare skill in mammals, and we have limited information about the contexts in which they use it. Previous studies suggested that cetaceans in general are skilled at imitating sounds, but only few species have been studied to date. To expand this investigation to another species and to investigate the possible influence of the social environment on vocal learning, we studied the whistle repertoire of a female Risso's dolphin (Grampus griseus) that was stranded at an early age and was subsequently raised in a group of bottlenose dolphins (Tursiops truncatus). We show that this cross-fostered animal produced vocal signals more akin to those of its Tursiops poolmates than those of Risso's dolphins in the wild. This is one of very few systematic cross-fostering studies in cetaceans and the first to suggest vocal production learning in the Risso's dolphin. Our findings also suggest that social experience is a major factor in the development of the vocal repertoire in this species.

Potential Uses of Anthropogenic Noise as a Source of Information in Animal Sensory and Communication Systems.

Although current research on the impact of anthropogenic noise has focused on the detrimental effects, there is a range of ways by which animals could benefit from increased noise levels. Here we discuss two potential uses of anthropogenic noise. First, local variations in the ambient-noise field could be used to perceive objects and navigate within an environment. Second, introduced sound cues could be used as a signal for prey detection or orientation and navigation. Although the disadvantages of noise pollution will likely outweigh any positive effects, it is important to acknowledge that such changes may benefit some species.

Multiple-Pulse Sounds and Seals: Results of a Harbor Seal (Phoca vitulina) Telemetry Study During Wind Farm Construction.

Offshore construction and survey techniques can produce pulsed sounds with a high sound pressure level. In coastal waters, the areas in which they are produced are often also used by seals, potentially resulting in auditory damage or behavioral avoidance. Here, we describe a study on harbor seals during a wind farm installation off southeast England. The study used GPS/global system for mobile communication tags on 23 harbor seals that provided distribution and activity data; the closest range of individual seals to piling varied from 6.65 to 46.1 km. Furthermore, the maximum predicted received levels (RLs) at individual seals varied between 146.9 and 169.4 dB re 1 µPa peak to peak.

Bottlenose dolphins can use learned vocal labels to address each other.

In animal communication research, vocal labeling refers to incidents in which an animal consistently uses a specific acoustic signal when presented with a specific object or class of objects. Labeling with learned signals is a foundation of human language but is notably rare in nonhuman communication systems. In natural animal systems, labeling often occurs with signals that are not influenced by learning, such as in alarm and food calling. There is a suggestion, however, that some species use learned signals to label conspecific individuals in their own communication system when mimicking individually distinctive calls. Bottlenose dolphins (Tursiops truncatus) are a promising animal for exploration in this area because they are capable of vocal production learning and can learn to use arbitrary signals to report the presence or absence of objects. Bottlenose dolphins develop their own unique identity signal, the signature whistle. This whistle encodes individual identity independently of voice features. The copying of signature whistles may therefore allow animals to label or address one another. Here, we show that wild bottlenose dolphins respond to hearing a copy of their own signature whistle by calling back. Animals did not respond to whistles that were not their own signature. This study provides compelling evidence that a dolphin's learned identity signal is used as a label when addressing conspecifics. Bottlenose dolphins therefore appear to be unique as nonhuman mammals to use learned signals as individually specific labels for different social companions in their own natural communication system.

Grey seals use anthropogenic signals from acoustic tags to locate fish: evidence from a simulated foraging task.

Anthropogenic noise can have negative effects on animal behaviour and physiology. However, noise is often introduced systematically and potentially provides information for navigation or prey detection. Here, we show that grey seals (Halichoerus grypus) learn to use sounds from acoustic fish tags as an indicator of food location. In 20 randomized trials each, 10 grey seals individually explored 20 foraging boxes, with one box containing a tagged fish, one containing an untagged fish and all other boxes being empty. The tagged box was found after significantly fewer non-tag box visits across trials, and seals revisited boxes containing the tag more often than any other box. The time and number of boxes needed to find both fish decreased significantly throughout consecutive trials. Two additional controls were conducted to investigate the role of the acoustic signal: (i) tags were placed in one box, with no fish present in any boxes and (ii) additional pieces of fish, inaccessible to the seal, were placed in the previously empty 18 boxes, making possible alternative chemosensory cues less reliable. During these controls, the acoustically tagged box was generally found significantly faster than the control box. Our results show that animals learn to use information provided by anthropogenic signals to enhance foraging success.

Come dine with me: food-associated social signalling in wild bottlenose dolphins (Tursiops truncatus).

Food-related signalling is widespread in the animal kingdom with some food-associated vocalizations considered functionally referential. Food calls can, however, vary greatly in the type of information they convey. Thus, there are a multitude of purposes for which food calls are used, including social recruitment, caller spacing, the indication of type, quantity, quality, divisibility of food, the caller's hunger level and even as tools to manipulate prey behaviour. Yet little work has focused on the social aspect of food calling in animals. We investigated the association of social signals in wild bottlenose dolphins with foraging behaviour where context-specific food-associated calls are commonly produced. Our data showed that specific social signals were significantly correlated with food call production and these calls rarely occurred in the absence of food calls. We suggest that animals are sharing additional information on the food patch itself with their social affiliates.

Common dolphin whistle responses to experimental mid-frequency sonar.

Oceanic delphinids that occur in and around Navy operational areas are regularly exposed to intense military sonar broadcast within the frequency range of their hearing. However, empirically measuring the impact of sonar on the behavior of highly social, free-ranging dolphins is challenging. Additionally, baseline variability or the frequency of vocal state-switching among social oceanic dolphins during undisturbed conditions is lacking, making it difficult to attribute changes in vocal behavior to anthropogenic disturbance. Using a network of drifting acoustic buoys in controlled exposure experiments, we investigated the effects of mid-frequency (3-4 kHz) active sonar (MFAS) on whistle production in short-beaked (Delphinus delphis delphis) and long-beaked common dolphins (Delphinus delphis bairdii) in southern California. Given the complexity of acoustic behavior exhibited by these group-living animals, we conducted our response analysis over varying temporal windows (10 min- 5 s) to describe both longer-term and instantaneous changes in sound production. We found that common dolphins exhibited acute and pronounced changes in whistle rate in the 5 s following exposure to simulated Navy MFAS. This response was sustained throughout sequential MFAS exposures within experiments simulating operational conditions, suggesting that dolphins may not habituate to this disturbance. These results indicate that common dolphins exhibit brief yet clearly detectable acoustic responses to MFAS. They also highlight how variable temporal analysis windows-tuned to key aspects of baseline vocal behavior as well as experimental parameters related to MFAS exposure-enable the detection of behavioral responses. We suggest future work with oceanic delphinids explore baseline vocal rates a-priori and use information on the rate of change in vocal behavior to inform the analysis time window over which behavioral responses are measured.

The effect of a startle-eliciting device on the foraging success of individual harbor seals (Phoca vitulina).

Pinniped predation on commercially and ecologically important prey has been a source of conflict for centuries. In the Salish Sea, harbor seals (Phoca vitulina) are suspected of impeding the recovery of culturally and ecologically critical Pacific salmon (Oncorhynchus spp.). In Fall 2020, a novel deterrent called Targeted Acoustic Startle Technology (TAST) was deployed at Whatcom Creek to deter harbor seals from preying on fall runs of hatchery chum (O. keta) and Chinook (O. tshawytscha) salmon in Bellingham, Washington, USA. Field observations were conducted in 2020 to compare the presence and foraging success of individual harbor seals across sound exposure (TAST-on) and control (TAST-off) conditions. Observations conducted the previous (2019) and following (2021) years were used to compare the effects observed in 2020 to two control years. Using photo-identification, individual seals were associated with foraging successes across all 3 years of the study. Generalized linear mixed models showed a significant 45.6% reduction in the duration (min) individuals remained at the creek with TAST on, and a significant 43.8% reduction in the overall foraging success of individuals. However, the observed effect of TAST varied across individual seals. Seals that were observed regularly within one season were more likely to return the year after, regardless of TAST treatment. Generalized linear models showed interannual variation in the number of seals present and salmon consumed. However, the effect of TAST in 2020 was greater than the observed variation across years. Our analyses suggest TAST can be an effective tool for managing pinniped predation, although alternate strategies such as deploying TAST longer-term and using multi-unit setups to increase coverage could help strengthen its effects. Future studies should further examine the individual variability found in this study.

Vocal copying of individually distinctive signature whistles in bottlenose dolphins.

Vocal learning is relatively common in birds but less so in mammals. Sexual selection and individual or group recognition have been identified as major forces in its evolution. While important in the development of vocal displays, vocal learning also allows signal copying in social interactions. Such copying can function in addressing or labelling selected conspecifics. Most examples of addressing in non-humans come from bird song, where matching occurs in an aggressive context. However, in other animals, addressing with learned signals is very much an affiliative signal. We studied the function of vocal copying in a mammal that shows vocal learning as well as complex cognitive and social behaviour, the bottlenose dolphin (Tursiops truncatus). Copying occurred almost exclusively between close associates such as mother-calf pairs and male alliances during separation and was not followed by aggression. All copies were clearly recognizable as such because copiers consistently modified some acoustic parameters of a signal when copying it. We found no evidence for the use of copying in aggression or deception. This use of vocal copying is similar to its use in human language, where the maintenance of social bonds appears to be more important than the immediate defence of resources.

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.

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.