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'.

Inter-group alliance dynamics in Indo-Pacific bottlenose dolphins (Tursiops aduncus).

The social intelligence hypothesis holds that complex social relationships are the major selective force underlying the evolution of large brain size and intelligence. Complex social relationships are exemplified by coalitions and alliances that are mediated by affiliative behavior, resulting in differentiated but shifting relationships. Male Indo-Pacific bottlenose dolphins in Shark Bay, Australia, form three alliance levels or 'orders', primarily among non-relatives. Strategic alliance formation has been documented within both first- and second-order alliances and between second-order alliances ('third-order alliances'), revealing that the formation of strategic inter-group alliances is not limited to humans. Here we conducted a fine-scale study on 22 adult males over a 6-year period to determine if third-order alliance relationships are differentiated, and mediated by affiliative interactions. We found third-order alliance relationships were strongly differentiated, with key individuals playing a disproportionate role in maintaining alliances. Nonetheless, affiliative interactions occurred broadly between third-order allies, indicating males maintain bonds with third-order allies of varying strength. We also documented a shift in relationships and formation of a new third-order alliance. These findings further our understanding of dolphin alliance dynamics and provide evidence that strategic alliance formation is found in all three alliance levels, a phenomenon with no peer among non-human animals.

Anthropogenic noise impairs cooperation in bottlenose dolphins.

Understanding the impact of human disturbance on wildlife populations is of societal importance,1 with anthropogenic noise known to impact a range of taxa, including mammals,2 birds,3 fish,4 and invertebrates.5 While animals are known to use acoustic and other behavioral mechanisms to compensate for increasing noise at the individual level, our understanding of how noise impacts social animals working together remains limited. Here, we investigated the effect of noise on coordination between two bottlenose dolphins performing a cooperative task. We previously demonstrated that the dolphin dyad can use whistles to coordinate their behavior, working together with extreme precision.6 By equipping each dolphin with a sound-and-movement recording tag (DTAG-37) and exposing them to increasing levels of anthropogenic noise, we show that both dolphins nearly doubled their whistle durations and increased whistle amplitude in response to increasing noise. While these acoustic compensatory mechanisms are the same as those frequently used by wild cetaceans,8,9,10,11,12,13 they were insufficient to overcome the effect of noise on behavioral coordination. Indeed, cooperative task success decreased in the presence of noise, dropping from 85% during ambient noise control trials to 62.5% during the highest noise exposure. This is the first study to demonstrate in any non-human species that noise impairs communication between conspecifics performing a cooperative task. Cooperation facilitates vital functions across many taxa and our findings highlight the need to account for the impact of disturbance on functionally important group tasks in wild animal populations.

An epigenetic DNA methylation clock for age estimates in Indo-Pacific bottlenose dolphins (Tursiops aduncus).

Knowledge of an animal's chronological age is crucial for understanding and predicting population demographics, survival and reproduction, but accurate age determination for many wild animals remains challenging. Previous methods to estimate age require invasive procedures, such as tooth extraction to analyse growth layers, which are difficult to carry out with large, mobile animals such as cetaceans. However, recent advances in epigenetic methods have opened new avenues for precise age determination. These 'epigenetic clocks' present a less invasive alternative and can provide age estimates with unprecedented accuracy. Here, we present a species-specific epigenetic clock based on skin tissue samples for a population of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia. We measured methylation levels at 37,492 cytosine-guanine sites (CpG sites) in 165 samples using the mammalian methylation array. Chronological age estimates with an accuracy of ±1 year were available for 68 animals as part of a long-term behavioral study of this population. Using these samples with known age, we built an elastic net model with Leave-One-Out-Cross-Validation, which retained 43 CpG sites, providing an r = 0.86 and median absolute age error (MAE) = 2.1 years (5% of maximum age). This model was more accurate for our data than the previously published methylation clock based on skin samples of common bottlenose dolphins (T. truncatus: r = 0.83, MAE = 2.2) and the multi-species odontocete methylation clock (r = 0.68, MAE = 6.8), highlighting that species-specific clocks can have superior performance over those of multi-species assemblages. We further developed an epigenetic sex estimator, predicting sex with 100% accuracy. As age and sex are critical parameters for the study of animal populations, this clock and sex estimator will provide a useful tool for extracting life history information from skin samples rather than long-term observational data for free-ranging Indo-Pacific bottlenose dolphins worldwide.

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.

Strategic intergroup alliances increase access to a contested resource in male bottlenose dolphins.

Efforts to understand human social evolution rely largely on comparisons with nonhuman primates. However, a population of bottlenose dolphins in Shark Bay, Western Australia, combines a chimpanzee-like fission-fusion grouping pattern, mating system, and life history with the only nonhuman example of strategic multilevel male alliances. Unrelated male dolphins form three alliance levels, or "orders", in competition over females: both within-group alliances (i.e., first- and second-order) and between-group alliances (third-order), based on cooperation between two or more second-order alliances against other groups. Both sexes navigate an open society with a continuous mosaic of overlapping home ranges. Here, we use comprehensive association and consortship data to examine fine-scale alliance relationships among 121 adult males. This analysis reveals the largest nonhuman alliance network known, with highly differentiated relationships among individuals. Each male is connected, directly or indirectly, to every other male, including direct connections with adult males outside of their three-level alliance network. We further show that the duration with which males consort females is dependent upon being well connected with third-order allies, independently of the effect of their second-order alliance connections, i.e., alliances between groups increase access to a contested resource, thereby increasing reproductive success. Models of human social evolution traditionally link intergroup alliances to other divergent human traits, such as pair bonds, but our study reveals that intergroup male alliances can arise directly from a chimpanzee-like, promiscuous mating system without one-male units, pair bonds, or male parental care.

Bottlenose dolphin communication during a role-specialized group foraging task.

A division of labor with role specialization is defined as individuals specializing in a subtask during repetitions of a group task. While this behavior is ubiquitous among humans, there are only four candidates found among non-eusocial mammals: lions, mice, chimpanzees, and bottlenose dolphins. Bottlenose dolphins in the Cedar Keys, Florida, engage in role specialized "driver-barrier feeding", where a "driver" dolphin herds mullet towards "barrier" dolphins. Thus trapped, the mullet leap out of the water where the dolphins catch them in air. To investigate whether dolphins use acoustic cues or signals to coordinate this behavior, vocalizations were recorded before and during driver-barrier feeding. Results of fine-scale audio and video analysis during 81 events by 7 different driver individuals suggest that barrier animals coordinate movements during these events by cueing on the driver's echolocation. Analysis of dolphin whistle occurrence before driving events versus another foraging technique, which does not involve role specialization, revealed significantly higher whistle production immediately prior to driver-barrier events. Possible whistle functions include signaling motivation, recruiting individuals to participate, and/or behavioral coordination. While the use of cues and signals is common in humans completing role-specialized tasks, this is the first study to investigate the use of vocalizations in the coordination of a role-specialized behavior in a non-human mammal.

Social integration influences fitness in allied male dolphins.

Understanding determinants of differential reproductive success is at the core of evolutionary biology because of its connection to fitness. Early work has linked variation in reproductive success to differences in age,1 rank,2 or size,3,4 as well as habitat characteristics.5 More recently, studies in group-living taxa have revealed that social relationships also have measurable effects on fitness.6-8 The influence of social bonds on fitness is particularly interesting in males who compete over reproductive opportunities. In Shark Bay, Western Australia, groups of 4-14 unrelated male bottlenose dolphins cooperate in second-order alliances to compete with rival alliances over access to females.9-12 Nested within second-order alliances, pairs or trios of males, which can vary in composition, form first-order alliances to herd estrus females. Using 30 years of behavioral data, we examined how individual social factors, such as first-order alliance stability, social connectivity, and variation in social bond strength within second-order alliances, affect male fitness. Analyzing the reproductive careers of 85 males belonging to 10 second-order alliances, we found that the number of paternities a male achieved was positively correlated with his cumulative social bond strength but negatively correlated with his variation in bond strength. Thus, well-integrated males with more homogeneous social bonds to second-order allies obtained most paternities. Our findings provide novel insights into the fitness benefits of polyadic cooperation among unrelated males and highlight the adaptive value of social bonds in this context.

Allied male dolphins use vocal exchanges to "bond at a distance".

Vocal interactions are intrinsic features of social groups and can play a pivotal role in social bonding.1,2 Dunbar's social bonding hypothesis posits that vocal exchanges evolved to "groom at a distance" when social groups became too large or complex for individuals to devote time to physical bonding activities.1,3 Tests of this hypothesis in non-human primates, however, suggest that vocal exchanges occur between more strongly bonded individuals that engage in higher grooming rates4-7 and thus do not provide evidence for replacement of physical bonding. Here, we combine data on social bond strength, whistle exchange frequency, and affiliative contact behavior rates to test this hypothesis in wild male Indo-Pacific bottlenose dolphins, who form multi-level alliances that cooperate over access to females.8-10 We show that, although whistle exchanges are more likely to occur within the core alliance, they occur more frequently between those males that share weaker social bonds, i.e., between core allies that spend less time together, while the opposite occurs for affiliative physical contact behavior. This suggests that vocal exchanges function as a low-cost mechanism for male dolphins that spend less time in close proximity and engage in fewer affiliative contact behaviors to reinforce and maintain their valuable alliance relationships. Our findings provide new evidence outside of the primate lineage that vocal exchanges serve a bonding function and reveal that, as the social bonding hypothesis originally suggested, vocal exchanges can function as a replacement of physical bonding activities for individuals to maintain their important social relationships.

Association patterns and community structure among female bottlenose dolphins: environmental, genetic and cultural factors.

Social structuring from assortative associations may affect individual fitness, as well as population-level processes. Gaining a broader understanding of social structure can improve our knowledge of social evolution and inform wildlife conservation. We investigated association patterns and community structure of female Indo-Pacific bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, assessing the role of kinship, shared culturally transmitted foraging techniques, and habitat similarity based on water depth. Our results indicated that associations are influenced by a combination of uni- and biparental relatedness, cultural behaviour and habitat similarity, as these were positively correlated with a measure of dyadic association. These findings were matched in a community level analysis. Members of the same communities overwhelmingly shared the same habitat and foraging techniques, demonstrating a strong homophilic tendency. Both uni- and biparental relatedness between dyads were higher within than between communities. Our results illustrate that intraspecific variation in sociality in bottlenose dolphins is influenced by a complex combination of genetic, cultural, and environmental aspects. Supplementary Information: The online version contains supplementary material available at 10.1007/s42991-022-00259-x.

Evidence that bottlenose dolphins can communicate with vocal signals to solve a cooperative task.

Cooperation experiments have long been used to explore the cognition underlying animals' coordination towards a shared goal. While the ability to understand the need for a partner in a cooperative task has been demonstrated in a number of species, there has been far less focus on cooperation experiments that address the role of communication. In humans, cooperative efforts can be enhanced by physical synchrony, and coordination problems can be solved using spoken language. Indeed, human children adapt to complex coordination problems by communicating with vocal signals. Here, we investigate whether bottlenose dolphins can use vocal signals to coordinate their behaviour in a cooperative button-pressing task. The two dolphin dyads used in this study were significantly more likely to cooperate successfully when they used whistles prior to pressing their buttons, with whistling leading to shorter button press intervals and more successful trials. Whistle timing was important as the dolphins were significantly more likely to succeed if they pushed their buttons together after the last whistle, rather than pushing independently of whistle production. Bottlenose dolphins are well known for cooperating extensively in the wild, and while it remains to be seen how wild dolphins use communication to coordinate cooperation, our results reveal that at least some dolphins are capable of using vocal signals to facilitate the successful execution of coordinated, cooperative actions.

Cooperation-based concept formation in male bottlenose dolphins.

In Shark Bay, Western Australia, male bottlenose dolphins form a complex nested alliance hierarchy. At the first level, pairs or trios of unrelated males cooperate to herd individual females. Multiple first-order alliances cooperate in teams (second-order alliances) in the pursuit and defence of females, and multiple teams also work together (third-order alliances). Yet it remains unknown how dolphins classify these nested alliance relationships. We use 30 years of behavioural data combined with 40 contemporary sound playback experiments to 14 allied males, recording responses with drone-mounted video and a hydrophone array. We show that males form a first-person social concept of cooperative team membership at the second-order alliance level, independently of first-order alliance history and current relationship strength across all three alliance levels. Such associative concepts develop through experience and likely played an important role in the cooperative behaviour of early humans. These results provide evidence that cooperation-based concepts are not unique to humans, occurring in other animal societies with extensive cooperation between non-kin.

Cooperative partner choice in multi-level male dolphin alliances.

Investigations into cooperative partner choice should consider both potential and realised partners, allowing for the comparison of traits across all those available. Male bottlenose dolphins form persisting multi-level alliances. Second-order alliances of 4-14 males are the core social unit, within which 2-3 males form first-order alliances to sequester females during consortships. We compared social bond strength, relatedness and age similarity of potential and realised partners of individual males in two age periods: (i) adolescence, when second-order alliances are formed from all available associates, and (ii) adulthood, when first-order allies are selected from within second-order alliances. Social bond strength during adolescence predicted second-order alliance membership in adulthood. Moreover, males preferred same-aged or older males as second-order allies. Within second-order alliances, non-mating season social bond strength predicted first-order partner preferences during mating season consortships. Relatedness did not influence partner choice on either alliance level. There is thus a striking resemblance between male dolphins, chimpanzees and humans, where closely bonded non-relatives engage in higher-level, polyadic cooperative acts. To that end, our study extends the scope of taxa in which social bonds rather than kinship explain cooperation, providing the first evidence that such traits might have evolved independently in marine and terrestrial realms.

The effects of exercise to promote quality of life in individuals with traumatic brain injuries: a systematic review.

OBJECTIVE: To systematically review the effects of exercise interventions that may enhance quality of life (QOL) in individuals with traumatic brain injury (TBI). METHODS: A systematic search was conducted using five databases up to April 2018. Studies were included if QOL was quantified following an exercise programme for people with a TBI. Methodological quality was assessed using a validated scoring checklist. Two independent reviewers assessed study inclusion and methodological quality. RESULTS: Thirteen studies met the inclusion criteria (seven RCTs, six non-RCTs). The median total scores for the quality assessment tool were 26.1 (RCTs), and 21.3 (non-RCTs), out of 33. Eight out of the 13 studies reported improved QOL following an exercise programme. The duration of the interventions varied from 8-12 weeks. The most common programmes involved moderate to vigorous exercise; with a frequency and duration of 3-5 times/week for 30-60 minutes. CONCLUSION: Due to the diversity of the exercise training interventions, heterogeneity of patient characteristics, multitude of QOL instruments and outcome domains assessed, it was not possible to draw any definitive conclusion about the effectiveness of exercise interventions. However, this review identified positive trends to enhance various aspects of QOL measured using a range of assessment tools.

Bias and Misrepresentation of Science Undermines Productive Discourse on Animal Welfare Policy: A Case Study.

Reliable scientific knowledge is crucial for informing legislative, regulatory, and policy decisions in a variety of areas. To that end, scientific reviews of topical issues can be invaluable tools for informing productive discourse and decision-making, assuming these reviews represent the target body of scientific knowledge as completely, accurately, and objectively as possible. Unfortunately, not all reviews live up to this standard. As a case in point, Marino et al.'s [1] review regarding the welfare of killer whales in captivity contains methodological flaws and misrepresentations of the scientific literature, including problematic referencing, overinterpretation of the data, misleading word choice, and biased argumentation. These errors and misrepresentations undermine the authors' conclusions and make it impossible to determine the true state of knowledge of the relevant issues. To achieve the goal of properly informing public discourse and policy on this and other issues, it is imperative that scientists and science communicators strive for higher standards of analysis, argumentation, and objectivity, in order to clearly communicate what is known, what is not known, what conclusions are supported by the data, and where we are lacking the data necessary to draw reliable conclusions.

Acoustic coordination by allied male dolphins in a cooperative context.

Synchronous displays are hallmarks of many animal societies, ranging from the pulsing flashes of fireflies, to military marching in humans. Such displays are known to facilitate mate attraction or signal relationship quality. Across many taxa, synchronous male displays appear to be driven by competition, while synchronous displays in humans are thought to be unique in that they serve a cooperative function. Indeed, it is well established that human synchrony promotes cooperative endeavours and increases success in joint action tasks. We examine another system in which synchrony is tightly linked to cooperative behaviour. Male bottlenose dolphins form long-lasting, multi-level, cooperative alliances in which they engage in coordinated efforts to coerce single oestrus females. Previous work has revealed the importance of motor synchrony in dolphin alliance behaviour. Here, we demonstrate that allied dolphins also engage in acoustic coordination whereby males will actively match the tempo and, in some cases, synchronize the production of their threat vocalization when coercing females. This finding demonstrates that male dolphins are capable of acoustic coordination in a cooperative context and, moreover, suggests that both motor and acoustic coordination are features of coalitionary behaviour that are not limited to humans.

Affiliation history and age similarity predict alliance formation in adult male bottlenose dolphins.

Male alliances are an intriguing phenomenon in the context of reproduction since, in most taxa, males compete over an indivisible resource, female fertilization. Adult male bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, form long-term, multilevel alliances to sequester estrus females. These alliances are therefore critical to male reproductive success. Yet, the long-term processes leading to the formation of such complex social bonds are still poorly understood. To identify the criteria by which male dolphins form social bonds with other males, we adopted a long-term approach by investigating the ontogeny of alliance formation. We followed the individual careers of 59 males for 14 years while they transitioned from adolescence (8-14 years of age) to adulthood (15-21 years old). Analyzing their genetic relationships and social associations in both age groups, we found that the vast majority of social bonds present in adolescence persisted through time. Male associations in early life predict alliance partners as adults. Kinship patterns explained associations during adolescence but not during adulthood. Instead, adult males associated with males of similar age. Our findings suggest that social bonds among peers, rather than kinship, play a central role in the development of adult male polyadic cooperation in dolphins.

Vocal behaviour of allied male dolphins during cooperative mate guarding.

Coercive mate guarding, where males use aggression to control female movements, is a form of sexual coercion which functions to constrain female mate choice. Non-human primates, for example, herd females to keep them away from competing males, but male bottlenose dolphins (Tursiops aduncus) also herd females to keep them close to their alliance partners. Indeed, pairs and trios of male dolphins work together to sequester single estrus females and defend them from competing alliances. Yet how males facilitate such coordination remains unknown. Here, we investigate the vocal behaviour of allied male bottlenose dolphins during the herding of individual females, examining how the production of whistles and 'pops' (a threat vocalisation) varied with behavioural state and inter-animal distances. Allied males produced both whistles and pops significantly more often and at higher rates during social interactions, though they differed in function. Whistle rates increased significantly when new individuals joined the consorting group, consistent with previous work showing that whistles are part of a greeting sequence for this species. Whistle matching also appeared to play a role in within-alliance coordination. Pop vocalisations increased significantly when the nearest male to the female changed, likely inducing the female to remain close as the males coordinate a guard switch. Building upon prior research examining female movements in response to pops, we show that males approach the female and current guard whilst popping, leading to a guard switch. Our results provide new insights into the use of vocal signals during cooperative mate guarding between allied male dolphins.

Multi-network-based diffusion analysis reveals vertical cultural transmission of sponge tool use within dolphin matrilines.

Behavioural differences among social groups can arise from differing ecological conditions, genetic predispositions and/or social learning. In the past, social learning has typically been inferred as responsible for the spread of behaviour by the exclusion of ecological and genetic factors. This 'method of exclusion' was used to infer that 'sponging', a foraging behaviour involving tool use in the bottlenose dolphin (Tursiops aduncus) population in Shark Bay, Western Australia, was socially transmitted. However, previous studies were limited in that they never fully accounted for alternative factors, and that social learning, ecology and genetics are not mutually exclusive in causing behavioural variation. Here, we quantified the importance of social learning on the diffusion of sponging, for the first time explicitly accounting for ecological and genetic factors, using a multi-network version of 'network-based diffusion analysis'. Our results provide compelling support for previous findings that sponging is vertically socially transmitted from mother to (primarily female) offspring. This research illustrates the utility of social network analysis in elucidating the explanatory mechanisms behind the transmission of behaviour in wild animal populations.

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.