Minding the Minds: A Primer on Cognitive Challenge for Marine Mammals in Human Care.

The past several decades have witnessed significant improvement in the physical welfare of marine mammals in zoos and aquariums. Over that same time period, research has revealed complex cognitive abilities in at least some of these species, yet there has been comparatively little attention paid to addressing their cognitive welfare per se. Studies primarily conducted with terrestrial animals have suggested that providing appropriate cognitive challenges in managed care settings can improve animal well-being. As a step toward facilitating this practice with marine mammals, this paper discusses factors relevant for creating appropriate cognitive challenges, outlines the three major categories of cognitive challenge that have been utilized with marine mammals, along with the logistical pros and cons of each, and calls on organizations that care for marine mammals to cultivate a bias for action with respect to providing cognitive care.

Are Dolphins Kept in Impoverished Environments?

Numerous studies have demonstrated the negative effects of impoverished environments versus the positive effects of enriched environments on animals' cognitive and neural functioning. Recently, a hypothesis was raised suggesting that conditions for dolphins in zoological facilities may be inherently impoverished, and thus lead to neural and cognitive deficits. This review directly examines that hypothesis in light of the existing scientific literature relevant to dolphin welfare in zoological facilities. Specifically, it examines how dolphins are housed in modern zoological facilities, where the characteristics of such housing fall on the continuum of impoverished-to-enriched environments, and the extent to which dolphins show behavioral evidence characteristic of living in impoverished environments. The results of this analysis show that contrary to the original hypothesis, modern zoological facilities do not inherently, or even typically, house dolphins in impoverished conditions. However, it also notes that there is variation in animal welfare across different zoological facilities, and that "not impoverished" would be a particularly low bar to set as an animal welfare standard. To optimize cognitive well-being, strategies for providing additional cognitive challenges for dolphins in zoological facilities are suggested.

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.

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.

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.

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.

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.

Making the strongest argument: Reply to Pepperberg (2015).

Jaakkola (2014) argued that because the majority of studies of animals' understanding of invisible displacement did not adequately control for the use of alternative lower-level strategies, clear and solid evidence for a conceptual understanding of invisible displacement existed only for great apes. Pepperberg (2015) takes issue with this conclusion with respect to Grey parrots. While I agree that olfactory and social cueing may not be issues of concern for parrots, I reiterate the need for a study that adequately controls for associative learning before we can confidently claim that parrots understand invisible displacement.

Do animals understand invisible displacement? A critical review.

The ability to mentally represent the movement of hidden objects (i.e., invisible displacement) is of theoretical importance due to its generally accepted status as an indicator of the development of a powerful type of representational capacity in human children. Over the past few decades, the understanding of invisible displacement has been claimed for a variety of animal species as well. However, a careful review of these studies finds that: (a) many were not properly blinded, (b) many did not properly control for lower-level associative strategies, and (c) success on simplified versions of the tasks can be explained by a simple attentional mechanism rather than by conceptual understanding. Indeed, when lower-level factors are controlled, evidence of understanding invisible displacement remains only for great apes.

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.