Modern day zoos and aquariums continuously assess the welfare of their animals and use evidence to make informed management decisions. Historically, many of the indicators of animal welfare used to assess the collection are negative indicators of welfare, such as stereotypic behavior. However, a lack of negative indicators of animal welfare does not demonstrate that an individual animal is thriving. There is a need for validated measures of positive animal welfare and there is a growing body of evidence that supports the use of behavioral diversity as a positive indicator of welfare. This includes an inverse relationship with stereotypic behavior as well as fecal glucocorticoid metabolites and is typically higher in situations thought to promote positive welfare. This review article highlights previous research on behavioral diversity as a potential positive indicator of welfare. Details are provided on how to calculate behavioral diversity and how to use it when evaluating animal welfare. Finally, the review will indicate how behavioral diversity can be used to inform an evidence-based management approach to animal care and welfare.

Cetaceans are long-lived, social species that are valued as ambassadors inspiring the public to engage in conservation action. Under professional care, they are critical partners with the scientific community to understanding the biology, behavior, physiology, health, and welfare requirements of this taxonomic group. The Cetacean Welfare Study was a highly collaborative research effort among zoos and aquariums accredited by the Alliance for Marine Mammal Parks and Aquariums and/or the Association of Zoos & Aquariums that provided important empirical and comparative information on the care and management of cetaceans. The goal was to identify factors that were related to the welfare of bottlenose dolphins and to develop reference intervals and values for common and novel indicators of health and welfare for common bottlenose dolphins (Tursiops truncatus), Indo-Pacific bottlenose dolphins (Tursiops aduncus), beluga whales (Delphinapterus leucas), and Pacific white-sided dolphins (Lagenorhynchus obliquidens). Data were collected from cetaceans at 43 accredited zoos and aquariums in seven countries in 2018 and 2019. This overview presents a summary of findings from the initial research articles that resulted from the study titled “Towards understanding the welfare of cetaceans in zoos and aquariums.” With multiple related objectives, animal-based metrics were used to advance frameworks of clinical care and target key conditions that were associated with good welfare of cetaceans in zoo and aquarium environments. As a result of this collaboration, species-specific reference intervals and values for blood variables and fecal hormone metabolites were developed and are freely available in an iOS application called ZooPhysioTrak. The results suggested that environmental enrichment programs and social management factors were more strongly related to behaviors likely indicative of positive welfare than habitat characteristics for common and Indo-Pacific bottlenose dolphins. These findings can be widely applied to optimize care and future science-based welfare practice.

In the wild, California sea lions (Zalophus californianus) are exposed to a wide variety of sensory information, which cannot be replicated in captive environments. Therefore, unique procedures are necessary for maintaining physiological and psychological health in nonhuman animals in captivity. The effects of introducing natural scents to captive enclosures have been investigated in a variety of species, yet they have not been examined in marine mammals. This project explored the behavioral effect of scent added to the environment, with the goal of improving the welfare of sea lions in captivity. Two scent types were introduced: (a) natural scents, found in their native environment, and (b) non-natural scents, not found in their native environment. This study examined not only scent enrichment but also the possible evolutionary underpinnings of pinniped olfaction. Scent enrichment was found to significantly impact sea lion behavior as demonstrated by a reduction in pattern swimming, an increase in habitat utilization, and a reduction in stereotypical behavior. However, there were no differences in behavior between natural and non-natural scent conditions.

High-resolution non-invasive cetacean tagging systems can be used to investigate the influence of habitat characteristics and management factors on behavior by quantifying activity levels and distance traveled by bottlenose dolphins (Tursiops truncatusandTursiops aduncus) in accredited zoos and aquariums. Movement Tags (MTags), a bio-logging device, were used to record a suite of kinematic and environmental information outside of formal training sessions as part of a larger study titled “Towards understanding the welfare of cetaceans in zoos and aquariums” (colloquially called the Cetacean Welfare Study). The purpose of the present study was to explore if and how habitat characteristics, environmental enrichment programs, and training programs were related to the distance traveled and energy expenditure of dolphins in accredited zoos and aquariums. Bottlenose dolphins in accredited zoos and aquariums wore MTags one day per week for two five-week data collection periods. Overall dynamic body acceleration (ODBA), a proxy for energy expenditure, and average distance traveled per hour (ADT) of 60 dolphins in 31 habitats were examined in relation to demographic, habitat, and management factors. Participating facilities were accredited by the Alliance for Marine Mammal Parks and/or Aquariums and the Association of Zoos & Aquariums. Two factors were found to be related to ADT while six factors were associated with ODBA. The results showed that enrichment programs were strongly related to both ODBA and ADT. Scheduling predictable training session times was also positively associated with ADT. The findings suggested that habitat characteristics had a relatively weak association with ODBA and were not related to ADT. In combination, the results suggested that management practices were more strongly related to activity levels than habitat characteristics.

Accredited zoos and aquariums continually strive to ensure high levels of animal welfare for the animals under their professional care. Best management practices include conducting research to better understand factors that lead to optimal welfare and then turning findings into practice. The current study is part of the larger Cetacean Welfare Study or more formally, “Towards understanding the welfare of cetaceans in zoos and aquariums.” Facilities participating in the study were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. Animal management factors and habitat characteristics were examined in relation to two potential indicators of welfare for common (Tursiops truncatus) and Indo-Pacific (Tursiops aduncus) bottlenose dolphins. Specifically, we examined environmental enrichment, animal training, and habitat characteristics that were significantly related to behavioral diversity and route tracing, a form of stereotypic behavior. Behavior was recorded from 47 animals at 25 facilities around the world. Overall, the rate of route tracing behavior observed during the study was very low and few animal management factors or habitat characteristics were found to be related to this behavior. One factor, enrichment diversity, had a significant positive relationship with route tracing and an inverse relationship with behavioral diversity. This finding may be a product of a response mounted by animal care specialists to the behavior as opposed to a cause. Animals that engaged in this behavior were likely provided more diverse enrichment in attempts to ameliorate the stereotypic behavior. However, multiple factors were found to significantly relate to behavioral diversity, a potential positive indicator of welfare for bottlenose dolphins. Dolphins that were trained on a predictable schedule had higher behavioral diversity than those on a semi-predictable schedule. There was a positive significant relationship between behavioral diversity and the number of habitats to which an animal had access, and a significant inverse relationship with the maximum depth of the habitat. Finally, animals that were split into groups and reunited or rotated between subgroups had higher behavioral diversity than animals managed in the same group. Information gained from the current study suggested that animal management techniques may be more important in ensuring good welfare for bottlenose dolphins than focusing on habitat size.

In recent decades, animal welfare science has evolved to utilize a multidisciplinary approach to assess the welfare of animals in accredited zoos and aquariums. Science-based animal welfare assessments have become an essential component of management programs and widespread application is expected by animal care professionals. Management practices for bottlenose dolphins in accredited facilities incorporate several programs that potentially impact animal welfare including environmental enrichment and animal training. Additionally, habitat characteristics, such as the dimensions of the habitat, have been proposed to affect welfare. While accredited facilities are required to meet high standards of care, habitat characteristics and management practices are not standardized across locations. Knowledge and subsequent application of these practices and habitat characteristics can enhance our understanding of factors associated with positive welfare. As part of a larger study of dolphin welfare titled “Towards understanding the welfare of cetaceans in zoos and aquariums” (colloquially called the Cetacean Welfare Study), survey data were collected from 86 bottlenose dolphins in 40 habitats at 38 facilities in seven countries. The major aims of this paper are to provide general descriptive information regarding dolphin management in accredited zoos and aquariums and to provide supplemental context to the other research published from the Cetacean Welfare Study data set. This paper provides a review of current habitat characteristics and management practices at those 38 accredited zoos and aquariums. These data enabled the identification and quantification of how cetacean management practices differed between participating facilities accredited by the Alliance for Marine Mammal Parks and Aquariums and the Association of Zoos & Aquariums. Variables were selected based on their potential association with welfare including the physical habitat, environmental enrichment, and training programs. The variables were also used for subsequent research in this collection of related papers to investigate important connections between potential indicators of welfare and habitat characteristics, environmental enrichment, and training programs.