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.

Total energy expenditure of bottlenose dolphins (Tursiops truncatus) of different ages.

Marine mammals are thought to have an energetically expensive lifestyle because endothermy is costly in marine environments. However, measurements of total energy expenditure (TEE; kcal day-1) are available only for a limited number of marine mammals, because large body size and inaccessible habitats make TEE measurements expensive and difficult to obtain for many taxa. We measured TEE in 10 adult common bottlenose dolphins (Tursiops truncatus) living in natural seawater lagoons at two facilities (Dolphin Research Center and Dolphin Quest) using the doubly labeled water method. We assessed the relative effects of body mass, age and physical activity on TEE. We also examined whether TEE of bottlenose dolphins, and more generally of marine mammals, differs from that expected for their body mass compared with other eutherian mammals, using phylogenetic least squares (PGLS) regressions. There were no differences in body mass or TEE (unadjusted TEE and TEE adjusted for fat-free mass) between dolphins from the two facilities. Our results show that adjusted TEE decreased and fat mass increased with age. Different measures of activity were not related to age, body fat or adjusted TEE. Both PGLS and the non-phylogenetic linear regression indicate that marine mammals have an elevated TEE compared with that of terrestrial mammals. However, bottlenose dolphins expended 17.1% less energy than other marine mammals of similar body mass. The two oldest dolphins (>40 years) showed a lower TEE, similar to the decline in TEE seen in older humans. To our knowledge, this is the first study to show an age-related metabolic decline in a large non-human mammal.

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.

Do dolphins really have a rightward lateralization for action? The importance of behavior-specific and orientation-neutral coding.

Because each side of the vertebrate body is controlled by a different side of the brain, studies of behavioral lateralization can provide insight into functional cerebral asymmetries in humans and other animals. The current study examined behavioral lateralization for a variety of behaviors in a group of 26 dolphins, in order to assess the claim that cetaceans show strong rightward action asymmetries indicative of a left-hemisphere specialization for action. We distinguished between side asymmetries and whole body turning actions, and devised a new coding system to counter the problem that previous studies of rolling behaviors (i.e., rotations around the long axis) have used contradictory coding systems depending on species' typical orientation. Our results did not support a generalized population-level rightward action asymmetry across multiple behaviors. Instead, we suggest that many dolphin behavioral asymmetries may be better explained as a result of perceptual processing asymmetries common across many vertebrates.

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.

Maternal signature whistle use aids mother-calf reunions in a bottlenose dolphin, Tursiops truncatus.

Individual vocal signatures play an important role in parent-offspring recognition in many animals. One species that uses signature calls to accurately facilitate individual recognition is the bottlenose dolphin. Female dolphins and their calves will use their highly individualised signature whistles to identify and maintain contact with one another. Previous studies have shown high signature whistle rates of both mothers and calves during forced separations. In more natural settings, it appears that the calf vocalises more frequently to initiate reunions with its mother. However, little is known about the mechanisms a female dolphin may employ when there is strong motivation for her to reunite with her calf. In this study, we conducted a series of experimental trials in which we asked a female dolphin to retrieve either her wandering calf or a series of inanimate objects (control). Our results show that she used her vocal signature to actively recruit her calf, and produced no such signal when asked to retrieve the objects. This is the first study to clearly manipulate a dolphin's motivation to retrieve her calf with experimental controls. The results highlight that signature whistles are not only used in broadcasting individual identity, but that maternal signature whistle use is important in facilitating mother-calf reunions.

Switching strategies: a dolphin's use of passive and active acoustics to imitate motor actions.

Scientists have long debated the extent to which animals can imitate. Observations of bottlenose dolphins suggest a sophisticated capacity for social imitation, but little is known about the nature of these abilities. Here, we explore the behavioral mechanisms underlying a dolphin's ability to copy motor actions while blindfolded (i.e., wearing eyecups). When a dolphin was asked to imitate a dolphin, a human, and then another dolphin blindfolded, his accuracy remained relatively consistent across models. However, his blindfolded echolocation dramatically increased when copying a human as compared to other dolphins, suggesting he actively switched between strategies: recognizing behaviors via characteristic sounds when possible, but via echolocation for the more novel sounding behaviors of the human. Such flexibility in changing perceptual routes demonstrates that the dolphin's imitation was not automatically elicited, but rather results from an intentional, problem-solving approach to imitation.

What do dolphins (Tursiops truncatus) understand about hidden objects?

Object permanence, the ability to mentally represent and reason about objects that have disappeared from view, is a fundamental cognitive skill that has been extensively studied in human infants and terrestrial animals, but not in marine animals. A series of four experiments examined this ability in bottlenose dolphins (Tursiops truncatus). After being trained on a "find the object" game, dolphins were tested on visible and invisible displacement tasks, and transpositions. In Experiments 1 and 2, dolphins succeeded at visible displacements, but not at invisible displacements or transpositions. Experiment 3 showed that they were able to pass an invisible displacement task in which a person's hand rather than a container was used as the displacement device. However, follow-up controls suggested they did so by learning local rules rather than via a true representation of the movement of hidden objects. Experiment 4 demonstrated that the dolphins did not rely on such local rules to pass visible displacement tasks. Thus, like many terrestrial animals, dolphins are able to succeed on visible displacement tasks, but seem unable to succeed on tasks requiring the tracking of hidden objects.

Understanding of the concept of numerically "less" by bottlenose dolphins (Tursiops truncatus).

In 2 experiments, bottlenose dolphins (Tursiops truncatus) judged the ordinal relationship between novel numerosities. The dolphins were first trained to choose the exemplar with the fewer number of items when presented with just a few specific comparisons (e.g., 2 vs. 6, 1 vs. 3, and 3 vs. 7). Generalization of this rule was then tested by presenting the dolphins with all possible pairwise comparisons between 1 and 8. The dolphins chose the exemplar with the fewer number of items at levels far above chance, showing that they could recognize and represent numerosities on an ordinal scale. Their pattern of errors was consistent with the idea of an underlying analog magnitude representation.