"Cognition in marine mammals: the strength of flexibility in adapting to marine life".

In this theme issue, our multidisciplinary contributors highlight the cognitive adaptations of marine mammals. The cognitive processes of this group are highly informative regarding how animals cope with specifics of and changes in the environment, because, not only did modern marine mammals evolve from numerous, non-related terrestrial animals to adapt to an aquatic lifestyle, but some of these species regularly move between two worlds, land and sea. Here, we bring together scientists from different fields and take the reader on a journey that begins with the ways in which modern marine mammals (whales, dolphins, seals, sea lions and manatees) utilize their perceptual systems, next moves into studies of the constraints and power of individuals' cognitive flexibility, and finally showcases how those systems are deployed in social and communicative contexts. Considering the cognitive processes of the different marine mammals in one issue from varying perspectives will help us understand the strength of cognitive flexibility in changing environments-in marine mammals and beyond.

Information-seeking across auditory scenes by an echolocating dolphin.

Dolphins gain information through echolocation, a publicly accessible sensory system in which dolphins produce clicks and process returning echoes, thereby both investigating and contributing to auditory scenes. How their knowledge of these scenes contributes to their echoic information-seeking is unclear. Here, we investigate their top-down cognitive processes in an echoic matching-to-sample task in which targets and auditory scenes vary in their decipherability and shift from being completely unfamiliar to familiar. A blind-folded adult male dolphin investigated a target sample positioned in front of a hydrophone to allow recording of clicks, a measure of information-seeking and effort; the dolphin received fish for choosing an object identical to the sample from 3 alternatives. We presented 20 three-object sets, unfamiliar in the first five 18-trial sessions with each set. Performance accuracy and click counts varied widely across sets. Click counts of the four lowest-performance-accuracy/low-discriminability sets (X = 41%) and the four highest-performance-accuracy/high-discriminability sets (X = 91%) were similar at the first sessions' starts and then decreased for both kinds of scenes, although the decrease was substantially greater for low-discriminability sets. In four challenging-but-doable sets, number of clicks remained relatively steady across the 5 sessions. Reduced echoic effort with low-discriminability sets was not due to overall motivation: the differential relationship between click number and object-set discriminability was maintained when difficult and easy trials were interleaved and when objects from originally difficult scenes were grouped with more discriminable objects. These data suggest that dolphins calibrate their echoic information-seeking effort based on their knowledge and expectations of auditory scenes.

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.

The Relevance of Ecological Transitions to Intelligence in Marine Mammals.

Macphail's comparative approach to intelligence focused on associative processes, an orientation inconsistent with more multifaceted lay and scientific understandings of the term. His ultimate emphasis on associative processes indicated few differences in intelligence among vertebrates. We explore options more attuned to common definitions by considering intelligence in terms of richness of representations of the world, the interconnectivity of those representations, the ability to flexibly change those connections, and knowledge. We focus on marine mammals, represented by the amphibious pinnipeds and the aquatic cetaceans and sirenians, as animals that transitioned from a terrestrial existence to an aquatic one, experiencing major changes in ecological pressures. They adapted with morphological transformations related to streamlining the body, physiological changes in respiration and thermoregulation, and sensory/perceptual changes, including echolocation capabilities and diminished olfaction in many cetaceans, both in-air and underwater visual focus, and enhanced senses of touch in pinnipeds and sirenians. Having a terrestrial foundation on which aquatic capacities were overlaid likely affected their cognitive abilities, especially as a new reliance on sound and touch, and the need to surface to breath changed their interactions with the world. Vocal and behavioral observational learning capabilities in the wild and in laboratory experiments suggest versatility in group coordination. Empirical reports on aspects of intelligent behavior like problem-solving, spatial learning, and concept learning by various species of cetaceans and pinnipeds suggest rich cognitive abilities. The high energy demands of the brain suggest that brain-intelligence relationships might be fruitful areas for study when specific hypotheses are considered, e.g., brain mapping indicates hypertrophy of specific sensory areas in marine mammals. Modern neuroimaging techniques provide ways to study neural connectivity, and the patterns of connections between sensory, motor, and other cortical regions provide a biological framework for exploring how animals represent and flexibly use information in navigating and learning about their environment. At this stage of marine mammal research, it would still be prudent to follow Macphail's caution that it is premature to make strong comparative statements without more empirical evidence, but an approach that includes learning more about how animals flexibly link information across multiple representations could be a productive way of comparing species by allowing them to use their specific strengths within comparative tasks.

Visual perception in a bottlenose dolphin (Tursiops truncatus): Successful recognition of 2-D objects rotated in the picture and depth planes.

Aquatic species such as bottlenose dolphins can move in 3 dimensions and frequently view objects from different orientations. This study examined their ability to identify 2-D objects visually despite changes in orientation across 2 rotation planes. A dolphin performed a matching-to-sample task in which a sample was presented at a different orientation from its match in a 3-alternative choice array. Samples were presented at 6 aspect angles in the picture plane (0°, ±45°, ±135°, 180°) and 6 aspect angles in the depth plane (0°, -45°, ±90°, +135°, 180°). Alternatives were always presented at 0°. Performance was significantly better than chance for all aspect angles in both rotation plane tests. There was a significant linear decline in accuracy as the sample object was rotated from 0° toward 180° in the picture plane. Performance with familiar objects (M = 97.1%) exceeded performance with novel objects (M = 76.9%). In the depth plane rotation test, there was a significant quadratic trend in accuracy as the sample object was rotated from 0° toward 180°, in which performance was significantly lower at ±90° than at all other orientations. Performance in the picture plane where all object features were available irrespective of orientation was significantly better than performance in the depth plane where the availability of visible features were dependent upon orientation (M = 81.2% vs. M = 63.0%). The dolphin's performance in this study shows evidence of both viewpoint-independent and viewpoint-dependent processes. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Consciousness in dolphins? A review of recent evidence.

For millennia, dolphins have intrigued humans. Scientific study has confirmed that bottlenose dolphins are large-brained, highly social mammals with an extended developmental period, flexible cognitive capacities, and powerful acoustic abilities including a sophisticated echolocation system. These findings have led some to ask if dolphins experience aspects of consciousness. Recent investigations targeting self-recognition/self-awareness and metacognition, constructs tied to consciousness on some accounts, have analyzed the dolphin's ability to recognize itself in a mirror or on a video as well as to monitor its own knowledge in a perceptual categorization task. The current article reviews this work with dolphins and grapples with some of the challenges in designing, conducting, and interpreting these studies as well as with general issues related to studying consciousness in animals. The existing evidence does not provide a convincing case for consciousness in dolphins. For productive scientific work on consciousness in dolphins (and other animals including humans), we need clearer characterizations of consciousness, better methods for studying it, and appropriate paradigms for interpreting outcomes. A current focus on metamemory in animals offers promise for future discovery in this area.

Whistle discrimination and categorization by the Atlantic bottlenose dolphin (Tursiops truncatus): a review of the signature whistle framework and a perceptual test.

Dolphin whistles vary by frequency contour, changes in frequency over time. Individual dolphins may broadcast their identities via uniquely contoured whistles, "signature whistles." A recent debate concerning categorization of these whistles has highlighted the on-going need for perceptual studies of whistles by dolphins. This article reviews research on dolphin whistles as well as presenting a study in which a captive, female, adult bottlenose dolphin performed a conditional matching task in which whistles produced by six wild dolphins in Sarasota Bay were each paired with surrogate producers, specific objects/places. The dolphin subject also categorized unfamiliar exemplars produced by the whistlers represented by the original stimuli. The dolphin successfully discriminated among the group of whistles, associated them with surrogate producers, grouped new exemplars of the same dolphin's whistle together when the contour was intact, and discriminated among same-contour whistles produced by the same dolphin. Whistle sequences that included partial contours were not categorized with the original whistlers. Categorization appeared to be based on contour rather than specific acoustic parameters or voice cues. These findings are consistent with the perceptual tenets associated with the signature whistle framework which suggests that dolphins use individualized whistle contours for identification of known conspecifics.

Human listeners provide insights into echo features used by dolphins (Tursiops truncatus) to discriminate among objects.

Echolocating bottlenose dolphins (Tursiops truncatus) discriminate between objects on the basis of the echoes reflected by the objects. However, it is not clear which echo features are important for object discrimination. To gain insight into the salient features, the authors had a dolphin perform a match-to-sample task and then presented human listeners with echoes from the same objects used in the dolphin's task. In 2 experiments, human listeners performed as well or better than the dolphin at discriminating objects, and they reported the salient acoustic cues. The error patterns of the humans and the dolphin were compared to determine which acoustic features were likely to have been used by the dolphin. The results indicate that the dolphin did not appear to use overall echo amplitude, but that it attended to the pattern of changes in the echoes across different object orientations. Human listeners can quickly identify salient combinations of echo features that permit object discrimination, which can be used to generate hypotheses that can be tested using dolphins as subjects.

Acoustic features of objects matched by an echolocating bottlenose dolphin.

The focus of this study was to investigate how dolphins use acoustic features in returning echolocation signals to discriminate among objects. An echolocating dolphin performed a match-to-sample task with objects that varied in size, shape, material, and texture. After the task was completed, the features of the object echoes were measured (e.g., target strength, peak frequency). The dolphin's error patterns were examined in conjunction with the between-object variation in acoustic features to identify the acoustic features that the dolphin used to discriminate among the objects. The present study explored two hypotheses regarding the way dolphins use acoustic information in echoes: (1) use of a single feature, or (2) use of a linear combination of multiple features. The results suggested that dolphins do not use a single feature across all object sets or a linear combination of six echo features. Five features appeared to be important to the dolphin on four or more sets: the echo spectrum shape, the pattern of changes in target strength and number of highlights as a function of object orientation, and peak and center frequency. These data suggest that dolphins use multiple features and integrate information across echoes from a range of object orientations.

Bottlenose dolphins perceive object features through echolocation.

How organisms (including people) recognize distant objects is a fundamental question. The correspondence between object characteristics (distal stimuli), like visual shape, and sensory characteristics (proximal stimuli), like retinal projection, is ambiguous. The view that sensory systems are 'designed' to 'pick up' ecologically useful information is vague about how such mechanisms might work. In echolocating dolphins, which are studied as models for object recognition sonar systems, the correspondence between echo characteristics and object characteristics is less clear. Many cognitive scientists assume that object characteristics are extracted from proximal stimuli, but evidence for this remains ambiguous. For example, a dolphin may store 'sound templates' in its brain and identify whole objects by listening for a particular sound. Alternatively, a dolphin's brain may contain algorithms, derived through natural endowments or experience or both, which allow it to identify object characteristics based on sounds. The standard method used to address this question in many species is indirect and has led to equivocal results with dolphins. Here we outline an appropriate method and test it to show that dolphins extract object characteristics directly from echoes.