The role of vocal learning in call acquisition of wild grey seal pups

This study was funded by the Natural Environment Research Council of the UK, grant no. NE/I024682/1.Pinnipeds have been identified as one of the best available models for the study of vocal learning. Experimental evidence for their learning skills is demonstrated with advanced copying skills, particularly in formant structure when copying human speech sounds and melodies. By contrast, almost no data are available on how learning skills are used in their own communication systems. We investigated the impact of playing modified seal sounds in a breeding colony of grey seals (Halichoerus grypus) to study how acoustic input influenced vocal development of eight pups. Sequences of two or three seal pup calls were edited so that the average peak frequency between calls in a sequence changed up or down. We found that seals copied the specific stimuli played to them and that copies became more accurate over time. The differential response of different groups showed that vocal production learning was used to achieve conformity, suggesting that geographical variation in seal calls can be caused by horizontal cultural transmission. While learning of pup calls appears to have few benefits, we suggest that it also affects the development of the adult repertoire, which may facilitate social interactions such as mate choice.Publisher PDFPeer reviewe

Vocal production learning in mammals revisited

Vocal production learning, the ability to modify the structure of vocalizations as a result of hearing those of others, has been studied extensively in birds but less attention has been given to its occurrence in mammals. We summarize the available evidence for vocal learning in mammals from the last 25 years, updating earlier reviews on the subject. The clearest evidence comes from cetaceans, pinnipeds, elephants and bats where species have been found to copy artificial or human language sounds, or match acoustic models of different sound types. Vocal convergence, in which parameter adjustments within one sound type result in similarities between individuals, occurs in a wider range of mammalian orders with additional evidence from primates, mole-rats, goats and mice. Currently, the underlying mechanisms for convergence are unclear with vocal production learning but also usage learning or matching physiological states being possible explanations. For experimental studies, we highlight the importance of quantitative comparisons of seemingly learned sounds with vocal repertoires before learning started or with species repertoires to confirm novelty. Further studies on the mammalian orders presented here as well as others are needed to explore learning skills and limitations in greater detail.Publisher PDFPeer reviewe

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

The project was funded by a BBSRC Studentship to S.L.K., and a Royal Society University Research Fellowship and a Fellowship of the Wissenschaftskolleg Berlin to V.M.J.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.PostprintPeer reviewe

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

Fieldwork for this study was funded by Harbor Branch Oceanographic Institution, Grossman Family Foundation, Dolphin Quest, Inc., NOAA Fisheries, Disney, the Office of Naval Research, Morris Animal Foundations Betty White Wildlife Rapid Response Fund, the Batchelor Foundation, and the Joint Industry Program.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.Publisher PDFPeer reviewe

Cross-modal perception of identity by sound and taste in bottlenose dolphins

Funding: The study was supported by a Marie Skłodowska-Curie fellowship of the European Commission, grant number 661214 (J.N.B. and V.M.J.)While studies have demonstrated concept formation in animals, only humans are known to label concepts to use them in mental simulations or predictions. To investigate whether other animals use labels comparably, we studied cross-modal, individual recognition in bottlenose dolphins (Tursiops truncatus) that use signature whistles as labels for conspecifics in their own communication. First, we tested whether dolphins could use gustatory stimuli and found that they could distinguish between water and urine samples, as well as between urine from familiar and unfamiliar individuals. Then, we paired playbacks of signature whistles of known animals with urine samples from either the same dolphin or a different, familiar animal. Dolphins investigated the presentation area longer when the acoustic and gustatory sample matched than when they mismatched. This demonstrates that dolphins recognize other individuals by gustation alone and can integrate information from acoustic and taste inputs indicating a modality independent, labeled concept for known conspecifics.Publisher PDFPeer reviewe

Cross-modal perception of identity by sound and taste in bottlenose dolphins

While studies have demonstrated concept formation in animals, only humans are known to label concepts to use them in mental simulations or predictions. To investigate whether other animals use labels comparably, we studied cross-modal, individual recognition in bottlenose dolphins (Tursiops truncatus) that use signature whistles as labels for conspecifics in their own communication. First, we tested whether dolphins could use gustatory stimuli and found that they could distinguish between water and urine samples, as well as between urine from familiar and unfamiliar individuals. Then, we paired playbacks of signature whistles of known animals with urine samples from either the same dolphin or a different, familiar animal. Dolphins investigated the presentation area longer when the acoustic and gustatory sample matched than when they mismatched. This demonstrates that dolphins recognize other individuals by gustation alone and can integrate information from acoustic and taste inputs indicating a modality independent, labeled concept for known conspecifics

Through the looking glass: how do marked dolphins use mirrors and what does it mean?

Funding: Studienstiftung des Deutschen Volkes; Deutsche Forschungsgemeinschaft (Gu227/16-1).Mirror-guided self-inspection is seen as a cognitive hallmark purportedly indicating the existence of self-recognition. Only a few species of great apes have been reported to pass a standard mark test for mirror self-recognition in which animals attempt to touch a mark. In addition, evidence for passing the mark test was also reported for Asian elephants, two species of corvids, and a species of cleaner fish. Mirror self-recognition has also been claimed for bottlenose dolphins, using exposure of marked areas to a mirror as evidence. However, what counts as self-directed behaviour to see the mark and what does not has been debated. To avoid this problem, we marked the areas around both eyes of the animals at the same time, one with visible and the other with transparent dye to control for haptic cues. This allowed the animal to see the mark easily and us to investigate what side was exposed to the mirror as an indicator for mark observation. We found that the animals actively chose to inspect their visibly marked side while they did not show an increased interest in a marked conspecific in the pool. These results demonstrate that dolphins use the mirror to inspect their marks and, therefore, likely recognise a distinction between self and others.Publisher PDFPeer reviewe

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

This study was funded by Marine Scotland (Scottish Government). Open Access funding provided by The University of St Andrews.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.Publisher PDFPeer reviewe

Vocal behaviour and feeding ecology of killer whales Orcinus orca around Shetland, UK

Killer whales Orcinus orca are sighted regularly off Shetland, UK, but little is known about their numbers, diet and population identity. We aimed to relate vocal behaviour to diet of killer whales around Shetland in order to investigate population structure and differences in feeding strategies. Fieldwork was conducted in the summers of 2008 and 2009. We located killer whales through a sightings network and shore-based scans and collected photo-ID data, behavioural information, feeding data and acoustic recordings from a small boat. The majority of encounters (n = 14) were of small groups (1 to 15 individuals) travelling close to shore and feeding on marine mammals. Two encounters were with large groups (20+ individuals) feeding on herring Clupea harengus farther offshore. Seal-hunting groups vocalised rarely, producing pulsed calls, echolocation clicks and whistles almost exclusively when surface-active or milling after a kill. Herring-eating groups were largely silent during one encounter, but very vocal during the other. Analysis of pulsed calls identified 6 stereotyped call types for seal-hunting groups and 7 for herring-eating groups. No call types were shared between both kinds of groups. The vocal behaviour of seal-hunting groups showed striking parallels to that of Pacific marine mammal specialists and presumably evolved to decrease detection by acoustically sensitive prey. One call type produced by Shetland herring-eating killer whales matched a vocalisation that a previous study had described from Iceland and identified as a possible herding call that may function to concentrate herring during feeding. These findings point to behavioural and dietary specialisation among Shetland killer whales, which should be taken into account when making management decisions affecting these animals

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

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Marine Mammal Science 29 (2013): 109–122, doi:10.1111/j.1748-7692.2011.00549.x.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, 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. Non-signature whistles occur over longer or shorter periods, 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.This work was supported by Dolphin Quest, National Oceanic and Atmospheric Administration (NOAA) Fisheries Service, Disney’s Animal Programs and Mote Marine Laboratory (R.S.W.), Harbor Branch Oceanographic Institute (L.S.S. and R.S.W.), and a Royal Society University Research Fellowship (V.M.J.)