Relationships between animal management and habitat characteristics with two potential indicators of welfare for bottlenose dolphins under professional care

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.

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Assessment of animal management and habitat characteristics associated with social behavior in bottlenose dolphins across zoological facilities

PLoS ONE ◽

10.1371/journal.pone.0253732 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0253732

Author(s):

Lance J. Miller ◽

Lisa K. Lauderdale ◽

Jill D. Mellen ◽

Michael T. Walsh ◽

Douglas A. Granger

Keyword(s):

Social Behavior ◽

Environmental Enrichment ◽

Bottlenose Dolphins ◽

Social Behaviors ◽

Habitat Characteristics ◽

Enrichment Programs ◽

Animal Management ◽

Social Species ◽

The Social ◽

Management Techniques

Bottlenose dolphins are a behaviorally complex, social species that display a variety of social behaviors. Because of this, it is important for zoological facilities to strive to ensure animals display species-appropriate levels of social behavior. The current study is part of the multi-institutional study entitled “Towards understanding the welfare of cetaceans in zoos and aquariums” commonly referred to as the Cetacean Welfare Study. All participating facilities were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. Behavioral data were collected on 47 bottlenose dolphins representing two subspecies, Tursiops truncatus and Tursiops aduncus, at 25 facilities. The social behaviors of group related activity (group active) as well as interacting with conspecifics (interact with conspecific) were examined for their relationships to both animal management factors and habitat characteristics. The behavioral state of group active and the rate of interact with conspecific were both positively related to the frequency of receiving new forms of environmental enrichment. Both were inversely related to the random scheduling of environmental enrichment. Additional results suggested interact with conspecific was inversely related with daytime spatial experience and that males displayed group active more than females. Overall, the results suggested that animal management techniques such as the type and timing of enrichment may be more important to enhance social behavior than habitat characteristics or the size of the habitat. Information gained from this study can help facilities with bottlenose dolphins manage their enrichment programs in relation to social behaviors.

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Bottlenose dolphin habitat and management factors related to activity and distance traveled in zoos and aquariums

PLoS ONE ◽

10.1371/journal.pone.0250687 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0250687

Author(s):

Lisa K. Lauderdale ◽

K. Alex Shorter ◽

Ding Zhang ◽

Joaquin Gabaldon ◽

Jill D. Mellen ◽

...

Keyword(s):

Energy Expenditure ◽

Environmental Enrichment ◽

Management Practices ◽

Average Distance ◽

Bottlenose Dolphins ◽

Training Session ◽

Habitat Characteristics ◽

Activity Levels ◽

Enrichment Programs ◽

Management Factors

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 truncatus and Tursiops 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.

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Behavioral diversity as a potential positive indicator of animal welfare in bottlenose dolphins

PLoS ONE ◽

10.1371/journal.pone.0253113 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0253113

Author(s):

Lance J. Miller ◽

Lisa K. Lauderdale ◽

Jocelyn L. Bryant ◽

Jill D. Mellen ◽

Michael T. Walsh ◽

...

Keyword(s):

Animal Welfare ◽

Inverse Relationship ◽

Diversity Index ◽

Bottlenose Dolphins ◽

Significant Inverse Relationship ◽

Behavioral Diversity ◽

Fecal Cortisol ◽

Professional Care ◽

And Behavior ◽

Positive Animal

Accredited zoological facilities are committed to fully understanding the behavioral, mental, and physical needs of each species to continuously improve the welfare of the animals under their professional care and detect when welfare has diminished. In order to accomplish this goal, internally consistent and externally valid indicators of animal welfare are necessary to advance our understanding of the current welfare status of individual animals. Historically, efforts have focused on monitoring visible or observable signs of poor health or problem behavior, but lack of signs or problems does not necessarily demonstrate that an individual animal is thriving. The current study examined fecal hormone metabolite levels and behavior for two species of bottlenose dolphins (Tursiops truncatus and Tursiops aduncus) from 25 different accredited zoological facilities. At the time of the study, all facilities were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. This was part of the multi-institutional study ‘Towards understanding of the welfare of cetaceans in zoos and aquariums” commonly referred to as the Cetacean Welfare Study. Behavioral diversity was calculated using the Shannon Diversity Index on species-appropriate behavioral events. Behavioral diversity was compared to the fecal metabolites of cortisol, aldosterone, and the ratio of cortisol to dehydroepiandrosterone (DHEA) as well as the stereotypic behavior of route tracing. Similar to previous studies on other species, there was a significant inverse relationship between behavioral diversity and both fecal cortisol metabolites and route tracing. Additionally, a significant inverse relationship also exists between behavioral diversity and the ratio of fecal cortisol to DHEA metabolites. Behavioral diversity and fecal aldosterone metabolites were not associated. Additional research is still needed to validate behavioral diversity as an indicator of positive animal welfare for bottlenose dolphins and across species. However, based on current results, facilities could utilize behavioral diversity combined with other measures of welfare to more comprehensively evaluate the welfare of bottlenose dolphins.

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Efficacy of an interactive apparatus as environmental enrichment for common bottlenose dolphins (Tursiops truncatus)

Animal Welfare ◽

10.7120/09627286.29.4.379 ◽

2020 ◽

Vol 29 (4) ◽

pp. 379-386

Author(s):

LK Lauderdale ◽

LJ Miller

Keyword(s):

Tursiops Truncatus ◽

Environmental Enrichment ◽

Bottlenose Dolphins ◽

Well Being ◽

Specific Behaviour ◽

Effective Form ◽

Professional Care ◽

Species Specific ◽

And Control ◽

Case Basis

Environmental enrichment is a key component in improving the psychological and physiological well-being of animals under professional care. Environmental enrichment involves the addition of stimuli, including objects and cognitive challenges, into the environment in order to increase species-specific behaviour and provide opportunities for choice and control. The effectiveness of enrichment should be evaluated on a case-by-case basis to determine if the desired result has been achieved. Environmental enrichment devices (EEDs) can be utilised to present novel problems to animals under professional care. Here, a submerged interactive cognitive apparatus was presented to eight bottlenose dolphins (Tursiops truncatus) five days a week for 18 weeks and behavioural indicators of animal welfare assessed. As a group, dolphins spent more time in social swims compared to solitary swims and more time at the bottom of the habitat than the middle or top throughout the day, even when the apparatus was not immediately available. Individuals' differences were apparent in the type and amount of engagement with the apparatus. Three dolphins engaged with the apparatus by solving it or consuming the reward. Two dolphins, D4 and D8, engaged simultaneously with the apparatus and participated in more social swimming with each other. D4 solved the interactive apparatus and engaged in more social active and solitary active behaviours. D1 and D4 increased their use of the bottom of the habitat. This study is the first report of underwater enrichment increasing dolphins time at depth throughout the day even when the enrichment device is not available. The interactive apparatus was an effective form of enrichment for dolphins participating in successful trials.

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Habitat characteristics and animal management factors associated with habitat use by bottlenose dolphins in zoological environments

PLoS ONE ◽

10.1371/journal.pone.0252010 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0252010

Author(s):

Lisa K. Lauderdale ◽

K. Alex Shorter ◽

Ding Zhang ◽

Joaquin Gabaldon ◽

Jill D. Mellen ◽

...

Keyword(s):

Environmental Enrichment ◽

Management Practices ◽

Training Programs ◽

Bottlenose Dolphins ◽

Habitat Characteristics ◽

Diving Behavior ◽

Weekly Schedule ◽

Single Group ◽

Enrichment Programs ◽

Group Welfare

The way an animal uses its habitat can serve as an indicator of habitat appropriateness for the species and individuals. Bottlenose dolphins (Tursiops truncatus and Tursiops aduncus) in accredited zoos and aquariums experience a range of habitat types and management programs that provide opportunities for dolphins to engage in species-appropriate behaviors and potentially influence their individual and group welfare. Data in the present study were collected as part of a larger study titled “Towards understanding the welfare of cetaceans in zoos and aquariums” (colloquially called the Cetacean Welfare Study). Non-invasive bio-logging devices (Movement Tags) recorded the diving behavior and vertical habitat movements of 60 bottlenose dolphins at 31 zoos and aquariums that were accredited by the Alliance for Marine Mammal Parks and Aquariums and/or the Association of Zoos & Aquariums. Bottlenose dolphins wore a Movement Tag one day per week for two five-week data collection periods. Demographic variables, environmental enrichment programs, training programs, and habitat characteristics were associated with habitat usage. Longer dive durations and use of the bottom third of the habitat were associated with higher enrichment program index values. Dolphins receiving new enrichment on a monthly/weekly schedule also used the bottom third of the habitat more often than those receiving new enrichment on a yearly/year+ schedule. Dolphins that were managed in a group that was split into smaller subgroups during the day and were reunited into one group at night spent less time in the top third of the habitat than those who remained in a single group with consistent members at all times. Dolphins that were managed as subgroups with rotating members but were never united as one group spent less time in the bottom third of the habitat than those who remained in a single group with consistent members at all times. Taken together, the results suggested that management practices, such as enrichment and training programs, played a greater role in how dolphins interacted with their environment relative to the physical characteristics of the habitat.

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Towards understanding the welfare of cetaceans in accredited zoos and aquariums

PLoS ONE ◽

10.1371/journal.pone.0255506 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0255506

Author(s):

Lisa K. Lauderdale ◽

Jill D. Mellen ◽

Michael T. Walsh ◽

Douglas A. Granger ◽

Lance J. Miller

Keyword(s):

Environmental Enrichment ◽

Research Effort ◽

Clinical Care ◽

Bottlenose Dolphins ◽

Reference Intervals ◽

Habitat Characteristics ◽

Delphinapterus Leucas ◽

Specific Reference ◽

Conservation Action ◽

Beluga Whales

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.

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Environmental enrichment, training, and habitat characteristics of common bottlenose dolphins (Tursiops truncatus) and Indo-Pacific bottlenose dolphins (Tursiops aduncus)

PLoS ONE ◽

10.1371/journal.pone.0253688 ◽

2021 ◽

Vol 16 (8) ◽

pp. e0253688

Author(s):

Lisa K. Lauderdale ◽

Michael T. Walsh ◽

Jill D. Mellen ◽

Douglas A. Granger ◽

Lance J. Miller

Keyword(s):

Animal Welfare ◽

Environmental Enrichment ◽

Management Practices ◽

Training Programs ◽

Bottlenose Dolphins ◽

Habitat Characteristics ◽

Standards Of Care ◽

Data Set ◽

Widespread Application ◽

And Training

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.

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Environmental enrichment delays the development of stereotypic behavior and reduces variability in behavioral experiments using California mice (Peromyscus californicus)

10.1101/2021.01.05.425454 ◽

2021 ◽

Author(s):

Vanessa Minie ◽

Stephanie Ramos-Maciel ◽

Emily Wright ◽

Radmila Petric ◽

Brian Trainor ◽

...

Keyword(s):

Environmental Enrichment ◽

Model Systems ◽

Stereotypic Behavior ◽

Psychiatric Disease ◽

Behavioral Experiments ◽

Environmental Complexity ◽

Preclinical Research ◽

Peromyscus Californicus ◽

Cage Size ◽

California Mice

AbstractDomesticated mice and rats have shown to be powerful model systems for biomedical research, but there are cases in which the biology of species is a poor match for the hypotheses under study. The California mouse (Peromyscus californicus) has unique physiological and behavioral traits and has emerged as a powerful model for studying sex differences in the biology of psychiatric disease, which is particularly relevant considering the new NIH guidelines that require the inclusion of sex as a biological variable. Despite its growing role in preclinical research, there is a lack of studies assessing species-specific housing needs, which presents a challenge for research facilities seeking to ensure good welfare and obtaining high-quality experimental data. Indeed, captive California mice present a high prevalence of stereotypic backflipping behavior, a common consequence of suboptimal housing and a potential source of experimental outcome variability. Using three different cage systems, the present studies show that increasing housing space as well as social and environmental complexity can delay the development of stereotypic behavior in male and female California mice. Critically, this reduction in stereotypy is accompanied by increased effect sizes of stress in an established model for social anxiety. These results suggest that increased cage size and enrichment could enhance welfare in California mice while simultaneously increasing the quality of behavioral experiments.

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