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.

Using Anticipatory Behavior to Detect the Change in Interest in an Activity Repeated Several Times and Avoid Habituation in Bottlenose Dolphins (Tursiops Truncatus).

Environmental enrichment is an essential component of the management policies used by zoos and aquaria to promote animals' welfare. However, when enrichments are provided several times, they can cause habituation and lose their enrichment effects. A simple method to avoid it could be making a preventive assessment about the trend of animals' interest in a stimulus provided several times. Here, we hypothesized that anticipatory behavior could be used to assess the decrease in interest in playing with objects when the activity is repeated. Moreover, we also assumed that this could be done before providing objects to play with. Our results support this hypothesis. Specifically, we found a positive correlation between the time the 7 dolphins tested spent performing anticipatory behavior before the enrichment sessions and the time they spent playing with objects during those sessions. As a result, anticipatory behavior performed before enrichment sessions predicted dolphins' interest in the session and allowed us to assess whether the sessions had lost their enrichment effect.

Benefit of Cognitive Environmental Enrichments on Social Tolerance and Play Behavior in Bottlenose Dolphins (Tursiops Truncatus).

Social tolerance is an essential feature of social life that can determine the good functioning of a group of animals. Play behaviors, like social play and playing with objects, are frequently associated with positive emotional and welfare states. As a result, zoos use various strategies to promote both social tolerance and play with objects. Providing animals with cognitive environmental enrichment can be an effective tool to achieve these goals. Here we tested whether cognitive environmental enrichment can promote social tolerance and play with objects in bottlenose dolphins (Tursiops truncatus). To this end, we provided a group of five dolphins with two types of cognitive enrichment: one for individual use and one for cooperative use, both based on the rope-pulling task paradigm. Then we evaluated whether social tolerance and play with objects had increased after we provided dolphins with the two enrichments. Our results go in this direction, showing that after we provided dolphins with the enrichments, their intolerance behaviors decreased, both during feeding sessions and play sessions, while their play with objects increased. As a result, the two enrichments we used could be useful for improving dolphins' housing conditions.

Cooperation increases bottlenose dolphins' (Tursiops truncatus) social affiliation.

Dolphins live in a fission-fusion society, where strong social bonds and alliances can last for decades. However, the mechanism that allows dolphins to form such strong social bonds is still unclear. Here, we hypothesized the existence of a positive feedback mechanism in which social affiliation promotes dolphins' cooperation, which in turn promotes their social affiliation. To test it, we stimulated the cooperation of the 11 dolphins studied by providing a cooperative enrichment tool based on a rope-pulling task to access a resource. Then we measured the social affiliation [simple ratio index (SRI)] of each possible pair of dolphins and evaluated whether it increased after cooperation. We also evaluated whether, before cooperation, pairs that cooperated had a higher SRI than those that did not cooperate. Our findings showed that the 11 cooperating pairs had significantly stronger social affiliation before cooperation than the 15 non-cooperating pairs. Furthermore, cooperating pairs significantly increased their social affiliation after cooperation, while non-cooperating pairs did not. As a result, our findings provide support to our hypothesis, and suggest that the previous social affiliation between dolphins facilitates cooperation, which in turn promotes their social affiliation.

Using Anticipatory Behavior as Preference Test in The Bottlenose Dolphin (Tursiops truncatus).

The preference tests have made a great contribution to promoting animal welfare. However, they are not always easily applicable and have some criticalities. Recently the anticipatory behavior has been used to detect the animals' preference. In this study, we attempted to investigate the relationship between preference and anticipatory behavior. To this end, we tested on a group of dolphins (Tursiops truncatus) whether, with anticipatory behavior, it is possible to distinguish the animals' preference for different objects and then use it as a preference test. Anticipatory behavior is exhibited throughout the animal kingdom, it is easy to induce and measure, and does not have the criticalities of other preference tests. Therefore, its use as preference test could facilitate the study of animals' preferences and contribute to the promotion of their welfare. Our results support the hypothesis of use anticipatory behavior as a preference test. In fact, dolphins have anticipated the arrival of objects highly preferred with a frequency three times higher than shown toward objects less preferred, providing further evidence of the correlation between anticipatory behavior and the animals' preference.

Episodic-like memory in common bottlenose dolphins.

Episodic memory involves the conscious recollection of personally experienced events, which has often been argued to be a uniquely human ability.1-5 However, evidence for conscious episodic recall in humans is centered around language-based reports. With no agreed upon non-linguistic behavioral makers of consciousness,6 episodic-like memory7 therefore represents the behavioral characteristics of human episodic memory, in the absence of evidence for subjective experience during recall. Here, we provide compelling evidence for episodic-like memory in common bottlenose dolphins (Tursiops truncatus), based on the incidental encoding and unexpected question paradigm.8 This methodology aims to capture the incidental encoding characteristic of human episodic memory, in that when we recall an experience, we remember information that was trivial at the time of encoding, but was encoded automatically.9 We show that dolphins are able to use incidentally encoded spatial ("where") and social ("who") information to solve an unexpected memory task, using only a single test trial per test type, which ensured that the dolphins did not have the opportunity to semantically learn "rules" to pass the test. All participating dolphins made correct choices in both the "where" and "who" tests. These results suggest that dolphins are capable of encoding, recalling, and accessing incidental information within remembered events, which is an ability indicative of episodic memory in humans. We argue that the complex socio-ecological background of dolphins may have selected for the ability to recall both spatial and social information in an episodic-like manner.

Vocal accommodation in penguins (Spheniscus demersus) as a result of social environment.

The ability to vary the characteristics of one's voice is a critical feature of human communication. Understanding whether and how animals change their calls will provide insights into the evolution of language. We asked to what extent the vocalizations of penguins, a phylogenetically distant species from those capable of explicit vocal learning, are flexible and responsive to their social environment. Using a principal components (PCs) analysis, we reduced 14 vocal parameters of penguin's contact calls to four PCs, each comprising highly correlated parameters and which can be categorized as fundamental frequency, formant frequency, frequency modulation, and amplitude modulation rate and duration. We compared how these differed between individuals with varying degrees of social interactions: same-colony versus different-colony, same colony over 3 years and partners versus non-partners. Our analyses indicate that the more penguins experience each other's calls, the more similar their calls become over time, that vocal convergence requires a long time and relative stability in colony membership, and that partners' unique social bond may affect vocal convergence differently than non-partners. Our results suggest that this implicit form of vocal plasticity is perhaps more widespread across the animal kingdom than previously thought and may be a fundamental capacity of vertebrate vocalization.

A fast technique to induce and measure anticipatory behavior in bottlenose dolphins (Tursiops truncatus).

Anticipatory behavior describes the actions taken to prepare for an upcoming event. It is considered a promising tool for welfare assessment, but it is not fully applied in zoos and other facilities. This is probably due to the need to train animals, which can take a long time and make its use impractical. In this work, we tested, on a group of six dolphins (Tursiops truncatus), the effectiveness of a new technique to induce and measure anticipatory behavior without training animals. Our results show how this new methodology, which we called The Fast Technique (TFT), has been able to induce and measure anticipatory behavior toward the event studied, i.e., the play sessions with objects (PSO). Furthermore, it has produced the same result obtained with The Classical Technique (TCT), which requires a training phase. Therefore, our finding demonstrates the efficacy of a new technique that could facilitate the use of anticipatory behavior for both research and animal welfare assessment protocols.

Cross-modal individual recognition in the African penguin and the effect of partnership.

An animal's ability to recognize another individual by matching their image to their voice suggests they form internal representations of other individuals. To what extent this ability, termed cross-modal individual recognition, extends to birds other than corvids is unknown. Here, we used an expectancy violation paradigm to determine whether a monogamous territorial seabird (Spheniscus demersus) can cross-modally recognize familiar conspecifics (partners or colony-mates). After pairs of penguins spent time together in an isolated area, one of the penguins was released from the area leaving the focal penguin alone. Subsequently, we played contact calls of the released penguin (congruent condition) or a different penguin (incongruent condition). After being paired with a colony-mate, focal penguins' response latency to the auditory stimulus was faster in the incongruent compared to congruent condition, indicating the mismatch violated their expectations. This behavioural pattern was not observed in focal penguins after being paired with their partner. We discuss these different results in the light of penguins' natural behaviour and the evolution of social communication strategies. Our results suggest that cross-modal individual recognition extends to penguins and reveals, in contrast with previously thought, that social communication between members of this endangered species can also use visual cues.

Behavioural Diversity Study in Bottlenose Dolphin (Tursiops truncatus) Groups and Its Implications for Welfare Assessments.

In the recent past, animal welfare studies have tried to determine the best animal welfare measures and indicators. Expression of behavioural diversity is considered a potential positive welfare indicator, and to the authors' knowledge, it has not been validated nor studied in cetaceans. For the first time, a behavioural diversity study on bottlenose dolphins (Tursiops truncatus) groups was conducted at six European facilities. The study was carried out by the animal care staff, biologists and veterinarians and included 54 dolphins housed in several group compositions at the different participating facilities. The goal of our study was to analyse behavioural diversity in bottlenose dolphins at the group level to investigate how particular factors might impact the diversity of behaviours within the group and to discuss its implications for dolphin welfare assessments. Eight factors (i.e., "observer location", "number of individuals", "age class", "sex", "social grouping", "presence/absence of leading male", "presence/absence of visitors" and "enrichment provision") impacted the behavioural diversity of the observed groups, while no significant impact of the factors "time of day" and "activity before/after observation" could be found. Our study showed the feasibility of this kind of approach for cetaceans under professional care and the relevance to considering this parameter in dolphin welfare studies, despite certain limitations that warrant further research.

Long-term stability of vocal individuality cues in a territorial and monogamous seabird.

The stability of individual acoustic features is fundamental in social species, and more importantly in monogamous and territorial species, showing long-term fidelity both to the partner and the breeding site. In this study, the stability over time of two discrete vocal types was investigated in the African penguin (Spheniscus demersus), a monogamous and territorial seabird. Contact calls and ecstatic display songs were recorded from an ex situ colony in 2017 and in 2020. For each vocalisation, we measured 14 spectral and temporal acoustic parameters related to both source and filter components. Two separate leave-one-out cross-validated Discriminant Function Analyses (DFA) were then performed, generating the discriminant functions from the vocalisations collected in 2017 to classify those recorded in 2020. The DFA correctly classified 62% of the contact calls (10 subjects) and 80.9% of the ecstatic display songs (seven subjects) according to the correct emitter, showing that acoustic cues to individuality encoded in both vocal types remained unchanged over four consecutive breeding seasons. We suggest that, in this monogamous and territorial bird species, individual acoustic stability could be selected for to identify groupmates and neighbours over the years and to help couples to reunite in consecutive breeding seasons, increasing individual fitness.

Do penguins' vocal sequences conform to linguistic laws?

Information compression is a general principle of human language: the most frequent words are shorter in length (Zipf's Law of Brevity) and the duration of constituents decreases as the size of the linguistic construct increases (Menzerath-Altmann Law). Vocal sequences of non-human primates have been shown to conform to both these laws, suggesting information compression might be a more general principle. Here, we investigated whether display songs of the African penguin, which mediate recognition, intersexual mate choice and territorial defence, conform with these laws. Display songs are long, loud sequences combining three types of syllables. We found that the shortest type of syllable was the most frequent (with the shortest syllable being repeated stereotypically, potentially favouring signal redundancy in crowded environments). We also found that the average duration of the song's constituents was negatively correlated with the size of the song (a consequence of increasing the relative number of the shortest syllable type, rather than reducing the duration across all syllable types, thus preserving the communication of size-related information in the duration of the longest syllable type). Our results provide the first evidence for conformity to Zipf's and Menzerath-Altmann Laws in the vocal sequences of a non-primate species, indicating that these laws can coexist with selection pressures specific to the species' ecology.