In pop pursuit: social bond strength predicts vocal synchrony during cooperative mate guarding in bottlenose dolphins.

Vocal communication is an emblematic feature of group-living animals, used to share information and strengthen social bonds. Vocalizations are also used to coordinate group-level behaviours in many taxa, but little is known of the factors that may influence vocal behaviour during cooperative acts. Allied male Indo-Pacific bottlenose dolphins (Tursiops aduncus) use the 'pop' vocalization as a coercive signal when working together to herd single oestrous females. Using long-term association and acoustic data, we examined the influence of social and non-social factors on pop use by allied male dolphins in this context. Neither pop rate nor pop bout duration were influenced by any of the factors examined. However, allied males with stronger social bonds engaged in higher rates of vocal synchrony; whereby they actively matched the timing of their pop production. Hence, social bond strength influenced pop use in a cooperative context, suggesting dual functions of pop use: to induce the female to remain close, and to promote social bond maintenance and cooperation among males. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Bottlenose dolphins are sensitive to human attentional features, including eye functionality.

The ability to attribute attentional states to other individuals is a highly adaptive socio-cognitive skill and thus may have evolved in many social species. However, whilst humans excel in this ability, even chimpanzees appear to not accurately understand how visual attention works, particularly in regard to the function of eyes. The complex socio-ecological background and socio-cognitive skill-set of bottlenose dolphins (Tursiops sp.), alongside the specialised training that captive dolphins typically undergo, make them an especially relevant candidate for an investigation into their sensitivity to human attentional states. Therefore, we tested 8 bottlenose dolphins on an object retrieval task. The dolphins were instructed to fetch an object by a trainer under various attentional state conditions involving the trainer's eyes and face orientation: 'not looking', 'half looking', 'eyes open', and 'eyes closed'. As the dolphins showed an increased latency to retrieve the object in conditions where the trainer's head and eyes cued a lack of attention to the dolphin, particularly when comparing 'eyes open' vs 'eyes closed' conditions, we demonstrate that dolphins can be sensitive to human attentional features, namely the functionality of eyes. This study supports growing evidence that dolphins possess highly complex cognitive abilities, particularly those in the social domain.

Cetacean responses to violation of expectation paradigm in a free-swim context.

The investigation of individual responses to unexpected stimuli or outcomes provides insights into basic cognitive processes, such as mental representations, emotional states of surprise, and detections of anomalies. Three experiments using a violation of expectation paradigm were conducted with 12 belugas and 17 bottlenose dolphins in managed care to test two classes of stimuli (humans and objects) in manipulated sequences of familiar and unfamiliar humans (Study 1, trainers and strangers), familiar and unfamiliar objects (Study 2, typical enrichment devices and new objects), and finally objects and humans (Study 3). Gaze durations were assessed for each condition in a given study during free-swim contexts. The results supported previous findings that visual stimuli, regardless of class, were stimulating and intriguing for both belugas and bottlenose dolphins. Belugas were more likely to gaze longer at human and object stimuli and tended to gaze longer at unexpected experiences than control or expected experiences. Bottlenose dolphins showed similar trends except when objects were involved. Individual variability was present for both species with some individuals showing stronger patterns of responses for expected experiences than others. After 2 years of intermittent experiments, belugas and bottlenose dolphins in managed care maintained their curiosity about visual stimuli, for which they received no primary reinforcement. Investigating responses to unexpected stimuli with animals in managed care may provide insight into how these animals respond to biologically relevant conditions, such as boat presence, predators, and unfamiliar conspecifics.

Social and vocal complexity in bottlenose dolphins.

Bottlenose dolphins are highly social, renowned for their vocal flexibility, and possess highly enlarged brains relative to their body size. Here, we discuss some of the defining features of bottlenose dolphin social and vocal complexity and place this in the context of their cognitive evolution.

Observing the nature of relationships in male bottlenose dolphins.

As long-term studies reveal, bottlenose dolphin communities comprise a complex network of individual relationships. Individuals form strong bonds (e.g., mother-calf or male partnerships), transient relationships, and also compete against each other for resources. Evidence of bonded partnerships is typically revealed by the years-long study of associations with repeated sightings. However, quickly determining which individuals have close affiliations would benefit both field researchers working to describe individual behavior as they engage in cognitive activities such as cooperative foraging as well as caregivers in zoos who must decide which individuals should be housed together. Observations in aquariums are well-suited for collecting long-term, detailed information on how pairs interact because subjects can always be found and their behavior both above and below the water can be seen well. These are conditions that are rare for most (but not all) ocean-based studies. We used multiple measures to detect affiliated behavior across several dimensions of pairwise affiliation. Specifically, we used association indices to measure the frequency of affiliative behavior, the symmetry of the partnership, the tenor of interactions, and the stability of which partners were strongly affiliated from year to year. Synchronous behavior and reciprocity in proximity-seeking are two examples of potential markers of an affiliative relationship where individual choices-to join, to move together, and to leave-are visible to observers. We found that the combined measures were effective at identifying one pair that maintained a strong, stable relationship across years, one individual that formed a moderately strong trio relationship with both members of the most-affiliated pair, and one individual who was more variable in his relationships. These social markers provide a means of rapidly identifying bonded males in both aquarium and ocean settings, particularly when long-term knowledge of individual histories is not available.

Testing use of the first multi-partner cognitive enrichment devices by a group of male bottlenose dolphins.

Alliance formation plays a crucial part in male dolphins' lives. These partnerships may last for decades or even for a lifetime; thus, partner choice and the maintenance of these relationships are both considered key components of alliance formation. In our previous investigations, pairs of adult male dolphins showed a high success rate in cooperative manipulation of a cognitive enrichment device. Here, we introduced two novel cognitive enrichment devices to the group of five dolphins, facilitating simultaneous actions for not only pairs, but for three or even four dolphins. The devices were made of PVC tubes, fittings and caps equipped with rope handles, creating a three-way (T-shape) and a four-way (TT-shape) device. The devices were filled with fish and ice and were designed to be opened by simultaneous pull of the handles. Both devices were tested in 12 trials (each lasted for 15 min), separately. Only one of the caps could be opened, the others were affixed with the position of the openable cap counter-balanced over the trials. Although the dolphins received no training regarding the manipulation of the devices, they were successful in cooperatively opening the three-way devices in 10/12 of trials (70% by two and 30% by three dolphins) and the four-way devices also in 10/12 trials (50% by two, 40% by three and 10% by four dolphins). The dolphins interacted with the devices during the entire testing time, and this was mostly spent in cooperative play (77% and 56% of the test duration with the three-way and four-way device, respectively). The majority of the cooperative play was observed between one particular pair of dolphins that was temporarily associated with a third or sometimes even with a fourth dolphin. These findings demonstrate the first successful use of multi-partner cooperative enrichment devices, providing information on the social organization of a male dolphin group.

Lifetime stability of social traits in bottlenose dolphins.

Behavioral phenotypic traits or "animal personalities" drive critical evolutionary processes such as fitness, disease and information spread. Yet the stability of behavioral traits, essential by definition, has rarely been measured over developmentally significant periods of time, limiting our understanding of how behavioral stability interacts with ontogeny. Based on 32 years of social behavioral data for 179 wild bottlenose dolphins, we show that social traits (associate number, time alone and in large groups) are stable from infancy to late adulthood. Multivariate analysis revealed strong relationships between these stable metrics within individuals, suggesting a complex behavioral syndrome comparable to human extraversion. Maternal effects (particularly vertical social learning) and sex-specific reproductive strategies are likely proximate and ultimate drivers for these patterns. We provide rare empirical evidence to demonstrate the persistence of social behavioral traits over decades in a non-human animal.

Integrating Genetic, Environmental, and Social Networks to Reveal Transmission Pathways of a Dolphin Foraging Innovation.

Cultural behavior, which is transmitted among conspecifics through social learning [1], is found across various taxa [2-6]. Vertical social transmission from parent to offspring [7] is thought to be adaptive because of the parental generation being more skilled than maturing individuals. It is found throughout the animal kingdom, particularly in species with prolonged parental care, e.g., [8, 9]. Social learning can also occur among members of the same generation [4, 10, 11] or between older, non-parental individuals and younger generations [7] via horizontal or oblique transmission, respectively. Extensive work on primate culture has shown that horizontal transmission of foraging behavior is biased toward species with broad cultural repertoires [12] and those with increased levels of social tolerance [13, 14], such as great apes. Vertical social transmission has been established as the primary transmission mechanism of foraging behaviors in the Indo-Pacific bottlenose dolphin (Tursiops aduncus) population of Shark Bay, Western Australia [6, 9, 15, 16]. Here, we investigated the spread of another foraging strategy, "shelling" [17], whereby some dolphins in this population feed on prey trapped inside large marine gastropod shells. Using a multi-network version of "network-based diffusion analysis" (NBDA), we show that shelling behavior spreads primarily through non-vertical social transmission. By statistically accounting for both environmental and genetic influences, our findings thus represent the first evidence of non-vertical transmission of a foraging tactic in toothed whales. This research suggests there are multiple transmission pathways of foraging behaviors in dolphins, highlighting the similarities between cetaceans and great apes in the nature of the transmission of cultural behaviors. VIDEO ABSTRACT.

Five members of a mixed-sex group of bottlenose dolphins share a stereotyped whistle contour in addition to maintaining their individually distinctive signature whistles.

Most commonly, animal communication systems are driven by shared call repertoires, with some individual distinctiveness encoded as a byproduct of voice cues. We provide evidence that bottlenose dolphins produce both individually distinctive whistles, and a shared whistle type. A stereotyped whistle contour (termed the group whistle) is shared by five bottlenose dolphins that have lived, worked, and traveled together for at least 21 years. These five dolphins are members of a group of eight dolphins that work as a specialized team for the Navy Marine Mammal Program. Each dolphin is routinely recorded during periods when an individual is isolated from the others in above ground pools as part of their routine training. Each of the eight dolphins has an individually distinctive signature whistle. In addition, at least five of these dolphins share a distinct non-signature whistle type. This shared whistle contour was produced an average of 22.4% +/- 9.0% of the time during periods in which individuals were isolated. During these isolations the signature whistle was produced an average of 42.9% +/- 11.9% of the time. This is consistent with decades of signature whistle research. A group of 10 naïve observers rated the similarity of the different whistle contours. The observers rated the group whistle contour produced by all five dolphins as highly similar (P < 0.01). Their ratings further showed that the signature whistles of the five dolphins were very different (P < 0.01). These findings were further supported by discriminant function analyses. That said, the shared whistle contours still exhibited individual differences which may allow conspecifics to identify the producer even when a whistle contour is shared among multiple dolphins. This is the first in-depth analysis of a non-signature whistle type shared among multiple conspecifics.

Testing use of a potential cognitive enrichment device by an Indo-Pacific bottlenose dolphin (Tursiops aduncus).

Cognitive enrichment aims to provide animals with opportunities to use their cognitive skills and to promote behaviors associated with positive wellbeing. Cooperation in mammals has been recorded during various behavioral contexts such as hunting, mating, playing, and parental care. Coordinated activity, often with some level of problem-solving action included, is required during cooperation. To investigate dolphins' ability for collaborative problem-solving, an enrichment device was introduced to two adult male Indo-Pacific bottlenose dolphins (Tursiops aduncus). The device contained fish and ice and was designed to be opened by simultaneously pulling on both ends. After repeated presentation, it became apparent that only one dolphin had active interest in the device. To facilitate opportunities for problem-solving by this individual, an alternative collaborator, a human partner, was provided. Still, both dolphins had access to the device throughout the entire experiment. After the first opening, the same dolphin was highly successful in collaborating with the human in both joined (93%) and delayed (100%) partner conditions. The device provided a novel opportunity for the dolphin to use his cognitive skills. Even though only one dolphin participated actively, both dolphins showed varying degrees of interest to the device throughout the study. Both dolphins spent an average of 48% and 16% of their time, respectively, with the device, which resulted in a significant decrease in their other two most frequently observed behaviors: swimming and poolside observation. As a novel cognitive challenge, the device may be considered as a type of cognitive enrichment.

Functions of post-conflict bystander affiliations toward aggressors and victims in bottlenose dolphins.

Post-conflict affiliations initiated by bystanders (bystander affiliation) toward aggressors or victims have been suggested to represent the function of conflict management in some social living species. However, the function of bystander affiliations toward aggressors and victims has not been examined in marine mammals. In the present study, we investigated the function of bystander affiliations to aggressors and victims in bottlenose dolphins: self-protection, the substitute of reconciliation, social facilitation and tension relief of opponents. These bystander affiliations did not reduce post-conflict attacks by former opponents against group members. Bystander affiliation to aggressors tended to be performed by a bystander who had an affiliative relationship with the aggressor but not with the victim. Bystander affiliation to victims also tended to be initiated by a bystander who had an affiliative relationship with the victim but not the aggressor and was close to former opponents at the end of aggressions. Affiliation among group members who stayed near former opponents during aggressions did not increase after aggressions compared to that under control conditions. Renewed aggressions between former opponents decreased after bystander affiliations in our previous study. Bystanders who showed social closeness to former opponents may initiate bystander affiliation toward their affiliative former opponents because they may feel emotion, such as anxiety and excitement, of former opponents. Bystander affiliation toward aggressors and victims may function as tension relief between former opponents. Bystanders of bottlenose dolphins, who may have a relaxed dominant style, might initiate post-conflict affiliation to affiliative individuals unaffected by the dominance relationships among them, unlike despotic species.

Kinship and reproductive condition correlate with affiliation patterns in female southern Australian bottlenose dolphins.

Social relationships in female mammals are usually determined by an interplay among genetic, endogenous, social and ecological factors that ultimately affect their lifetime reproductive success. However, few studies have attempted to control for, and integrate these factors, hampering our understanding of drivers underlying female sociality. Here, we used generalized affiliation indices, combined with social networks, reproductive condition, and genetic data to investigate drivers of associations in female southern Australian bottlenose dolphins. Our analysis is based on photo-identification and genetic data collected through systematic boat surveys over a two-year study period. Female dolphins formed preferred associations and social clusters which ranged from overlapping to discrete home ranges. Furthermore, matrilineal kinship and biparental relatedness, as well as reproductive condition, correlated with the strength of female affiliations. In addition, relatedness for both genetic markers was also higher within than between social clusters. The predictability of resources in their embayment environment, and the availability of same-sex relatives in the population, may have favoured the formation of social bonds between genetically related females and those in similar reproductive condition. This study highlights the importance of genetic, endogenous, social and ecological factors in determining female sociality in coastal dolphins.

Directional hearing sensitivity for 2-30 kHz sounds in the bottlenose dolphin (Tursiops truncatus).

Bottlenose dolphins (Tursiops truncatus) depend on sounds at frequencies lower than 30 kHz for social communication, but little information on the directional dependence of hearing thresholds for these frequencies exists. This study measured underwater behavioral hearing thresholds for 2, 10, 20, and 30 kHz sounds projected from eight different positions around dolphins in both the horizontal and vertical planes. The results showed that the sound source direction relative to the dolphin affected hearing threshold, and that directional characteristics of the receiving beam pattern were frequency dependent. Hearing thresholds obtained from two adult dolphins demonstrated a positive relationship between directivity of hearing and stimulus frequency, with asymmetric receiving beam patterns in both the horizontal and vertical planes. Projecting sound from directly behind the dolphin resulted in frequency-dependent increases in hearing threshold up to 18.5 dB compared to when sound was projected in front. When the projector was situated above the dolphin thresholds were approximately 8 dB higher as compared to below. This study demonstrates that directional hearing exists for lower frequencies than previously expected.

Memory for own behaviour in pinnipeds.

Pinnipeds are aquatic predators feeding on a vast range of prey, and their social behaviour differs greatly between species (from extreme polygyny in some sea lions to monogamy in some true seals). It has been hypothesised that the foraging and social complexity of their lifestyle should drive the evolution of their cognitive abilities. To investigate how aware pinnipeds are of their own behaviour, a grey seal (Halichoerus grypus), two harbour seals (Phoca vitulina) and four South American sea lions (Otaria flavescens) were trained to repeat their own behaviour on command. Three already trained behaviours were used, and the animal was asked to repeat the behaviour twice to ensure that the animal recalled its own behaviour and not the command given for the previous behaviour. All three species could recall their own behaviour significantly better than by chance. The duration for which the animals could recall their behaviour was tested using a staircase paradigm. A delay was implemented between the completion of the behaviour and the command to repeat it. The delay was increased after correct responses and decreased after incorrect responses. The performance of all species fell towards chance level after 12-18 s, with no significant difference between species. These results indicate that sea lions and true seals are aware of their own behaviour and that true seals have similar short-term memory abilities. It also shows that pinnipeds have less developed short-term memory abilities compared to other aquatic predators, such as the bottlenose dolphin. The complexity of pinniped foraging and social behaviour does not seem to have driven the evolution of short-term memory abilities in these animals but might have contributed to their ability to recall their own behaviour.

Bottlenose dolphins do not behave prosocially in an instrumental helping task.

Although bottlenose dolphins (Tursiops truncatus) are known for being a highly social species that live in complex societies that rely on coalition formation and cooperative behaviours, experimental studies on prosocial behaviour in this species are scarce. Helping others reach their goals (instrumental helping) is considered as an example of prosocial behaviour. Thus, in this pilot study, we examined whether a group of five captive bottlenose dolphins would behave prosocially in an instrumental helping task. Dolphins were given the opportunity to share tokens that allow their partners to obtain a preferred toy. Dolphins were tested in their free time and they could choose to share the tokens or do nothing. None of the dolphins shared the tokens, instead, they preferred to play with them, ignoring their partners. They did transfer the tokens to other sides of the pool but out of the reach of their partners. Therefore, this group of dolphins did not spontaneously help their partners in this task, showing no preference for other-regarding behaviour in this context.

Jittered echo-delay resolution in bottlenose dolphins (Tursiops truncatus).

Psychophysical methods similar to those employed with bats were used to examine jittered echo-delay resolution in bottlenose dolphins (Tursiops truncatus). Two dolphins were trained to produce echolocation clicks and report a change from electronic echoes with a fixed delay of ~ 12.6 ms (~ 9.4 m simulated range) to echoes with delays that alternated (jittered) between successive emitted signals. Jitter delays varied from 0 to 50 µs. Jittered echo-delay thresholds were between 1 and 2 µs-the lowest achievable (non-zero) values with the hardware configuration. Error functions matched the click autocorrelation function near zero jitter delay, and were well within the envelope of the autocorrelation function; however, measured jitter delay thresholds were larger than predictions for a coherent or semicoherent receiver at comparable signal-to-noise ratios. When one of the two alternating jittered echoes was inverted in polarity, both dolphins reliably discriminated echoes at all jittered echo delays, including 0 µs (i.e., only jittering in polarity, not delay). Finally, both dolphins used unusual patterns of click emissions, where groups of echolocation clicks were interspersed with silent gaps. Further tests with sub-microsecond jitter values and various echo signal-to-noise ratios would be necessary for proper direct comparison with jitter detection values obtained for bats.

Bottlenose dolphins can understand their partner's role in a cooperative task.

In recent decades, a number of studies have examined whether various non-human animals understand their partner's role in cooperative situations. Yet the relatively tolerant timing requirements of these tasks make it theoretically possible for animals to succeed by using simple behavioural strategies rather than by jointly intended coordination. Here we investigated whether bottlenose dolphins could understand a cooperative partner's role by testing whether they could learn a button-pressing task requiring precise behavioural synchronization. Specifically, members of cooperative dyads were required to swim across a lagoon and each press their own underwater button simultaneously (within a 1 s time window), whether sent together or with a delay between partners of 1-20 s. We found that dolphins were able to work together with extreme precision even when they had to wait for their partner, and that their coordination improved over the course of the study, with the time between button presses in the latter trials averaging 370 ms. These findings show that bottlenose dolphins can learn to understand their partner's role in a cooperative situation, and suggest that the behavioural synchronization evident in wild dolphins' synchronous movement and coordinated alliance displays may be a generalized cognitive ability that can also be used to solve novel cooperative tasks.

Tail walking in a bottlenose dolphin community: the rise and fall of an arbitrary cultural 'fad'.

Social learning of adaptive behaviour is widespread in animal populations, but the spread of arbitrary behaviours is less common. In this paper, we describe the rise and fall of a behaviour called tail walking, where a dolphin forces the majority of its body vertically out of the water and maintains the position by vigourously pumping its tail, in a community of Indo-Pacific bottlenose dolphins (Tursiops aduncus). The behaviour was introduced into the wild following the rehabilitation of a wild female individual, Billie, who was temporarily co-housed with trained dolphins in a dolphinarium. This individual was sighted performing the behaviour seven years after her 1988 release, as was one other female dolphin named Wave. Initial production of the behaviour was rare, but following Billie's death two decades after her release, Wave began producing the behaviour at much higher rates, and several other dolphins in the community were subsequently sighted performing the behaviour. Social learning is the most likely mechanism for the introduction and spread of this unusual behaviour, which has no known adaptive function. These observations demonstrate the potential strength of the capacity for spontaneous imitation in bottlenose dolphins, and help explain the origin and spread of foraging specializations observed in multiple populations of this genus.

Bottlenose dolphin (Tursiops truncatus) discrimination of harmonic stimuli with range-dependent signal degradation.

The importance of perceived sound source distance has been noted in controlled exposure studies with free-ranging marine mammals. Different behavioral reactions have been observed for sonar exposures with a similar received level but differing source distances. This psychophysical study examined bottlenose dolphins' use of range-dependent acoustic features in classifying frequency-modulated tonal stimuli (∼10-kHz fundamental). Repetitive tones with simulated range-dependent high-frequency attenuation (HFA) and reverberation (REV) were presented with roving levels (levels varied ±10 dB). The dolphins were trained to produce a phonic response upon hearing tones simulating relatively distant 30-km sources and to withhold response for closer-range tones. Once this behavior was reliably performed, probe trials with intermediate ranges were used to examine stimulus classification based on HFA and REV. Dolphins responded to nearly all probe trials with ranges of 10 and 20 km, while responses were less frequent at 1 and 2 km. Probes with HFA and REV decoupled from simulated source distance indicated that the dolphins used HFA to a greater degree than REV in response decisions. These results suggest that dolphins can classify harmonic signals based on range-dependent HFA and REV independent of received level, making these cues potentially useful in deciding behavioral reactions to acoustic sources.

Bottlenose Dolphins Retain Individual Vocal Labels in Multi-level Alliances.

Cooperation between allied individuals and groups is ubiquitous in human societies, and vocal communication is known to play a key role in facilitating such complex human behaviors [1, 2]. In fact, complex communication may be a feature of the kind of social cognition required for the formation of social alliances, facilitating both partner choice and the execution of coordinated behaviors [3]. As such, a compelling avenue for investigation is what role flexible communication systems play in the formation and maintenance of cooperative partnerships in other alliance-forming animals. Male bottlenose dolphins in some populations form complex multi-level alliances, where individuals cooperate in the pursuit and defense of an important resource: access to females [4]. These strong relationships can last for decades and are critical to each male's reproductive success [4]. Convergent vocal accommodation is used to signal social proximity to a partner or social group in many taxa [5, 6], and it has long been thought that allied male dolphins also converge onto a shared signal to broadcast alliance identity [5-8]. Here, we combine a decade of data on social interactions with dyadic relatedness estimates to show that male dolphins that form multi-level alliances in an open social network retain individual vocal labels that are distinct from those of their allies. Our results differ from earlier reports of signature whistle convergence among males that form stable alliance pairs. Instead, they suggest that individual vocal labels play a central role in the maintenance of differentiated relationships within complex nested alliances.