Juvenile social play predicts adult reproductive success in male bottlenose dolphins.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins (Tursiops aduncus) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success.

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.

Aggressive interactions influence cognitive performance in Western Australian magpies.

Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.

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.

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.

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.

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.

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.

Cooperation or dolphin 'tug-of-war'? Comment on Kuczaj et al. and Eskelinen et al.

Two recent papers by Kuczaj et al. (Anim Cognit 18:543-550, 2015) and Eskelinen et al. (Anim Cognit 19:789-797, 2016) claim to have demonstrated that (i) bottlenose dolphins (Tursiops truncatus) cooperated to solve a novel task and (ii) vocal signals were important for coordinating these cooperative efforts. Although it is likely that bottlenose dolphins may share communicative signals in order to achieve a common goal, we suggest that this has not been demonstrated in the aforementioned studies. Here, we discuss the two main problems that preclude any definitive conclusions being drawn on cooperative task success and vocal communication from these studies. The first lies in the experimental design. The 'cooperative task', involving an apparatus that requires two dolphins to pull in opposite directions in order to achieve a food reward, is not conducive to cooperation, but could instead reflect a competitive 'tug-of-war'. It is therefore of questionable use in distinguishing competitive from cooperative interactions. Second, the suggestion that the occurrence of burst-pulsed signals in this task was indicative of cooperation is disputable, as (i) this study could not determine which dolphins were actually producing the signals and (ii) this sound type is more commonly associated with aggressive signalling in dolphins. We commend the authors for investigating this exciting and topical area in animal communication and cognition, but the question of whether dolphins cooperate and communicate to solve a cooperative task remains as yet unanswered.

Vocal matching: the what, the why and the how.

Over the years, vocal matching has progressed beyond being an interesting behavioural phenomenon to one that now has relevance to a wide range of fields. In this review, we use birds and cetaceans to explain what vocal matching is, why animals vocally match and how vocal matching can be identified. We show that while the functional aspects of vocal matching are similar, the contexts in which matching is used can differ between taxa. Whereas vocal matching in songbirds facilitates mate attraction and the immediate defence of resources, in parrots and cetaceans it plays a role in the maintenance of social bonds and the promotion of behavioural synchrony. We propose criteria for defining vocal matching with the aim of stimulating more matching studies across a wider range of taxa, including those using other, non-vocal, communication modalities. Finally, we encourage future studies to explore the importance of vocal learning in the development of vocal matching, and the information it may provide to third parties in the communication network.

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.

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.

You talkin' to me? Interactive playback is a powerful yet underused tool in animal communication research.

Over the years, playback experiments have helped further our understanding of the wonderful world of animal communication. They have provided fundamental insights into animal behaviour and the function of communicative signals in numerous taxa. As important as these experiments are, however, there is strong evidence to suggest that the information conveyed in a signal may only have value when presented interactively. By their very nature, signalling exchanges are interactive and therefore, an interactive playback design is a powerful tool for examining the function of such exchanges. While researchers working on frog and songbird vocal interactions have long championed interactive playback, it remains surprisingly underused across other taxa. The interactive playback approach is not limited to studies of acoustic signalling, but can be applied to other sensory modalities, including visual, chemical and electrical communication. Here, I discuss interactive playback as a potent yet underused technique in the field of animal behaviour. I present a concise review of studies that have used interactive playback thus far, describe how it can be applied, and discuss its limitations and challenges. My hope is that this review will result in more scientists applying this innovative technique to their own study subjects, as a means of furthering our understanding of the function of signalling interactions in animal communication systems.

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'.

Paneth cells expand from newly created and preexisting cells during repair after doxorubicin-induced damage.

Paneth cell numbers increase following intestinal damage, but mechanisms driving this process are not understood. We hypothesized that the increase in Paneth cell numbers is due to recruitment of cells from a preexisting pool of secretory progenitors. Mice were given a single injection of doxorubicin (Dox), and intestinal tissue was collected 0-168 h after treatment. Paneth, goblet, and intermediate cells were counted and evaluated for cell morphology. Quantitative RT-PCR was used to measure expression of various genes associated with Paneth cell allocation and maturation. Paneth cells were birth dated using incorporation of thymidine analogs given before or after Dox. Staining revealed "intermediate" cells, which were rarely observed in control crypts but increased significantly in number 96 and 120 h after Dox treatment. Birth dating of intermediate cells 5 days after Dox treatment revealed that 24% of these cells took up thymidine analog given prior to Dox treatment and 36% took up thymidine analog given after Dox treatment. Quantitative RT-PCR demonstrated a significant increase in Spdef, Atoh1, Sox9, EphB3, Mist, Wnt5a, FGF-9, and FGF-18 mRNAs and a significant decrease in Indian hedgehog mRNA. Expansion of the Paneth cell compartment after Dox treatment is due to generation of new cells and recruitment of cells from an existing pool. These cells express Paneth and goblet biomarkers and are found only during repair. Expansion of these cells correlates temporally with reduced Indian hedgehog and increased FGF and Wnt mRNA. These findings are significant, as they provide a first step in understanding mechanisms of Paneth cell expansion during mucosal repair.

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.

Small intestinal stem cells.

PURPOSE OF REVIEW: To summarize our current understanding of small intestinal stem cell biology and the current tools available for studying intestinal stem cells (ISCs). RECENT FINDINGS: Recent reviews and original reports point toward the presence of two distinct populations of stem cells (ISCs) within the intestinal crypts. Until recently, the study of these two populations has been hindered by the lack of biomarkers available for isolation and characterization of ISCs and the absence of suitable culture conditions for expansion of ISCs in vitro. With the accumulation of various surface markers and transgenic mouse models, we have been able to gain a better understanding of the genetic signature of ISCs. In addition, these tools have provided opportunities to begin to study how ISCs are influenced by the various components of the ISC niche, including fibroblasts, bacteria, lymphoid cells, and Paneth cells. Advances in culture conditions now allow for the establishment of in-vitro studies of ISC function and dynamics. SUMMARY: This brief review provides a general historical perspective of our understanding of the delineation of the two ISC populations. Furthermore, it discusses the known ISC markers and how these markers have been used to isolate and characterize ISC populations.

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.