Survival improvements of marine mammals in zoological institutions mirror historical advances in human longevity.

An intense public debate has fuelled governmental bans on marine mammals held in zoological institutions. The debate rests on the assumption that survival in zoological institutions has been and remains lower than in the wild, albeit the scientific evidence in support of this notion is equivocal. Here, we used statistical methods previously applied to assess historical improvements in human lifespan and data on 8864 individuals of four marine mammal species (harbour seal, Phoca vitulina; California sea lion, Zalophus californianus; polar bear, Ursus maritimus; common bottlenose dolphin, Tursiops truncatus) held in zoos from 1829 to 2020. We found that life expectancy increased up to 3.40 times, and first-year mortality declined up to 31%, during the last century in zoos. Moreover, the life expectancy of animals in zoos is currently 1.65-3.55 times longer than their wild counterparts. Like humans, these improvements have occurred concurrently with advances in management practices, crucial for population welfare. Science-based decisions will help effective legislative changes and ensure better implementation of animal care.

Cognitive judgement bias is associated with frequency of anticipatory behavior in bottlenose dolphins.

Many animals display a suite of increased vigilance and/or activity responses in relation to upcoming events, termed "anticipatory behavior." Anticipatory behavior toward positive events has been suggested as a cross-species measure of affective state as it likely reflects the balance of the reward-sensitivity system: various studies suggest that animals in poorer welfare situations show higher or excessive levels of anticipation for positive events. Another tool for evaluating animals' affective state is cognitive bias testing, and although it has been attempted, a link has not yet been made between cognitive bias and anticipatory behavior levels. Bottlenose dolphins (Tursiops truncatus) in captivity increase the performance of behaviors such as surface-looking and spy-hopping in anticipation of training sessions during which food is provided. In this study we measured anticipatory behavior frequency in bottlenose dolphins prior to positive reinforcement training sessions, and assessed whether frequency of anticipatory behavior correlated with their performance on cognitive bias tasks. We found that higher frequencies of anticipatory behavior for training sessions was significantly associated with more pessimistic judgements in cognitive bias tests, supporting previous findings linking higher reward sensitivity with negative affective states. Anticipatory behavior is an easily measured activity and could represent a welfare indicator in dolphins as well as other animals in captive environments.

Dolphin-WET-Development of a Welfare Evaluation Tool for Bottlenose Dolphins (Tursiops truncatus) under Human Care.

Ensuring high standards of animal welfare is not only an ethical duty for zoos and aquariums, but it is also essential to achieve their conservation, education, and research goals. While for some species, animal welfare assessment frameworks are already in place, little has been done for marine animals under human care. Responding to this demand, the welfare committee of the European Association for Aquatic Mammals (EAAM) set up a group of experts on welfare science, cetacean biology, and zoo animal medicine across Europe. Their objective was to develop a comprehensive tool to evaluate the welfare of bottlenose dolphins (Tursiops truncatus), named Dolphin-WET. The tool encompasses 49 indicators that were either validated through peer review or management-based expertise. The first of its kind, the Dolphin-WET is a species-specific welfare assessment tool that provides a holistic approach to evaluating dolphin welfare. Inspired by Mellor's Five Domains Model and the Welfare Quality®, its hierarchical structure allows for detailed assessments from overall welfare down to specific indicators. Through combining 37 animal-based and 12 resource-based indicators that are evaluated based on a two- or three-level scoring, the protocol offers a detailed evaluation of individual dolphins. This approach allows for regular internal monitoring and targeted welfare management, enabling caretakers to address specific welfare concerns effectively.

Cognitive Foraging Enrichment (but Not Non-Cognitive Enrichment) Improved Several Longer-Term Welfare Indicators in Bottlenose Dolphins.

Bottlenose dolphins are the most common cetacean kept globally in zoos and aquaria (hereafter zoos), and are gregarious animals with a mostly opportunistic, generalist feeding strategy in the wild. In zoos, they have limited to no opportunities to express natural foraging behaviours as they receive their daily food ration of dead fish in a series of training sessions. Enrichment provision has increased in recent years, but items are still predominantly simple and floating in nature, and do not always target the animals' problem-solving or food-acquisition behaviours. These discrepancies run concurrently with the intense debate about dolphin welfare in zoos and how to improve it. The current study used a within-subject design on 11 bottlenose dolphins at Kolmårdens Djurpark and measured how several welfare indicators differed between two treatments of "cognitive" and "non-cognitive" food-based enrichment. The treatments were provided on an alternating basis for eight consecutive weeks: during cognitive enrichment weeks, the animals received items which stimulated their problem-solving and foraging behaviours, and during non-cognitive enrichment weeks, they received simple items paired with fish (to eliminate bias due to food value). Data were taken related to several multidisciplinary welfare parameters during enrichment provision and training sessions, and to activity budget behaviours throughout the week. During the cognitive as opposed to non-cognitive enrichment weeks, the dolphins engaged more with the enrichment, were more motivated to participate in training sessions and performed less anticipatory and stereotypic behaviours, suggesting that cognitive enrichment improved several indicators of bottlenose dolphin welfare. Valuable lines of further investigation would be to understand how individual differences and different types of cognitive enrichment impact potential welfare benefits. Our results suggest that enrichment items promoting cognitive foraging behaviours may improve dolphin welfare, and therefore zoos might prioritise giving cognitive enrichment to this species as well as considering the same for other species with similar cognitive skills and foraging ecologies.

Increasing the Awareness of Animal Welfare Science in Marine Mammal Conservation: Addressing Language, Translation and Reception Issues.

Integrating welfare principles into conservation strategy is an emerging synthesis that encourages consideration of individual animals' quality of life in research, policies and law. However, these principles have gained limited traction in marine compared to terrestrial animal conservation. This manuscript investigates several factors that may be contributing to this disparity. In order to gauge current understanding of animal welfare science principles by marine mammal researchers and other stakeholders, a "Welfare in the Wild" workshop was convened at the 32nd European Cetacean Society conference (La Spezia, Italy, April 2018). The workshop was attended by 30 participants who completed pre- and post-workshop surveys on animal welfare principles. The survey results highlight a range of different views about exactly what animal welfare science is and how it can be applied to marine mammals. Specifically, participants' definitions appeared to vary depending on the type of employment or research they engaged in, indicating a need for an interdisciplinary common language. Secondly, we analysed the peer-reviewed literature in order to ascertain where marine mammal publications exploring welfare were being published. From 1950 to July 2020, a total of 299 articles featured both marine mammal taxa (one or more) and the word welfare in the title, abstract or keywords. This represents just 0.96% of the total peer-reviewed published papers on marine mammal taxa (n = 31,221) during the same period. When examining articles published within "Welfare and Ethics" (n = 6133) and "Aquatic-focused" (n = 139,352) journals, just 1.2% (n = 71) and 0.04% (n = 57) of articles, respectively, featured the word welfare when examining marine mammals. With the aim of exploring how explicitly including welfare evaluations in marine mammal research and management can benefit conservation outcomes, we framed our workshop and quantitative literature review findings to provide practical solutions to the language, translation and reception issues of this burgeoning cross-disciplinary collaboration.

Dolphins' Willingness to Participate (WtP) in Positive Reinforcement Training as a Potential Welfare Indicator, Where WtP Predicts Early Changes in Health Status.

Welfare science has built its foundations on veterinary medicine and thus measures of health. Since bottlenose dolphins (Tursiops truncatus) tend to mask symptoms of poor health, management in captivity would benefit from advanced understanding on the links between health and behavioural parameters, and few studies exist on the topic. In this study, four representative behavioural and health measures were chosen: health status (as qualified by veterinarians), percentage of daily food eaten, occurrences of new rake marks (proxy measure of social activity), and willingness to participate (WtP) in Positive Reinforcement Training sessions as qualitatively measured by their caretakers. These data were collected multiple times a day, every day over the course of a year from a multi-facility, large sample size (n dolphins = 51), allowing powerful analyses of the relationships between measures. First, it was found that dolphins with a higher WtP score also had a significantly better health status, ate a higher percentage of their daily food, and a lower occurrence of new rake marks. In addition, the WtP score was significantly lower up to 3 days before the weekly veterinary diagnosis of a decrease in health state; the percentage of daily food eaten and new rake mark measures did not show any significant change before such a diagnosis. These results suggest that WtP in training sessions is a potential behavioural measure of dolphin welfare, and an indicator of early changes in the dolphins' health state. We therefore suggest measurement of WtP as a more practical and non-invasive tool to support veterinary care and general management. More work needs to be conducted to elucidate the influence of social behaviour on health, and to identify other potential welfare indicators, but this long-term study has shown that qualitative measures can be both practical and valid when assessing dolphin welfare.

Cognitive Bias in Zoo Animals: An Optimistic Outlook for Welfare Assessment.

Cognitive bias testing measures how emotional states can affect cognitive processes, often described using the “glass half-full/half-empty” paradigm. Classical or operant conditioning is used to measure responses to ambiguous cues, and it has been reported across many species and contexts that an animal’s cognitive bias can be directly linked to welfare state, e.g., those in better welfare make more optimistic judgements. Cognitive bias testing has only recently been applied to animals and represents a key milestone in welfare science: it is currently one of the only accurate methods available to measure welfare. The tests have been conducted on many farm, laboratory, and companion animal species, but have only been carried out in zoo settings a handful of times. The aims of this review are to evaluate the feasibility of cognitive bias testing in zoos and its potential as a tool for studying zoo animal welfare. The few existing zoo cognitive bias studies are reviewed, as well as those conducted on similar, non-domesticated species. This work is then used to discuss how tests could be successfully designed and executed in zoo settings, which types of tests are most appropriate in different contexts, and how the data could be used to improve animal welfare. The review closely examines the many variables are present in the zoo which cannot be controlled as in other settings, termed here the Zoo Environment (ZE) Variables. It is recommended that tests are developed after consideration of each of the ZE Variables, and through strong collaboration between zookeepers, managers, and academic institutions. There is much unexplored potential of cognitive bias testing in the zoo setting, not least its use in investigating animal welfare in zoos. It is hoped that this review will stimulate increased interest in this topic from zoo managers, scientists, and industry regulators alike.

Bottlenose dolphins engaging in more social affiliative behaviour judge ambiguous cues more optimistically.

Cognitive bias tests measure variation in emotional appraisal and are validated methods to assess animals' affective states. However, the link between social behaviours and cognitive bias has not yet been investigated. Bottlenose dolphins are a gregarious species for whom welfare research is increasing in importance, and thus are a good model to test such an association. We adapted a spatial location judgement bias test for eight captive bottlenose dolphins to investigate the link between cognitive bias and social behaviour, where we conducted behavioural observations outside of training sessions and did not experimentally induce an affective state. Subjects showed stable individual differences in cognitive biases across the three test days. Furthermore, dolphins showing more synchronous swimming, a fundamental affiliative behaviour, judged ambiguous cues significantly more optimistically. Our longer-term data showed cognitive bias and synchronous swimming frequency were significantly associated for up to two months preceding the test, but disappeared prior to that, suggesting that here cognitive bias differences were reflected by transitory affective states rather than longer-term traits. We hypothesise that the frequency of synchronous swimming may induce affective states and/or be induced by them; either way, it has strong potential as an indicator of affective state in this species and beyond.

Schedule of human-controlled periods structures bottlenose dolphin (Tursiops truncatus) behavior in their free-time.

Behavioral patterns are established in response to predictable environmental cues. Animals under human care frequently experience predictable, human-controlled events each day, but very few studies have questioned exactly how behavioral patterns are affected by such activities. Bottlenose dolphins (Tursiops truncatus) maintained for public display are good models to study such patterns since they experience multiple daily human-controlled periods (e.g., shows, training for shows, medical training). Thus, we investigated the effect of training session schedule on their "free-time" behavior, studying 29 individuals within 4 groups from 3 European facilities. Our initial time budget analyses revealed that among the behaviors studied, dolphins spent the most time engaged in synchronous swimming, and within this category swam most at slow speeds and in close proximity to each other. "Slow-close" synchronous swimming peaked shortly after training sessions and was low shortly before the next session. Play behavior had significantly higher frequencies in juveniles than in adults, but the effect was only seen during the in-between session period (interval neither shortly before nor after sessions). Anticipatory behavior toward sessions was significantly higher shortly before sessions and lower afterward. We conclude that dolphin behaviors unconnected to the human-controlled periods were modulated by them: slow-close synchronous swimming and age-dependent play, which have important social dimensions and links to welfare. We discuss potential parallels to human-controlled periods in other species, including humans themselves. Our findings could be taken into account when designing welfare assessments, and aid in the provision of enrichment and maintaining effective schedules beneficial to animals themselves. (PsycINFO Database Record