Welfare Assessment Tools in Zoos: From Theory to Practice.

Zoos are increasingly implementing formalized animal welfare assessment programs to allow monitoring of welfare over time, as well as to aid in resource prioritization. These programs tend to rely on assessment tools that incorporate resource-based and observational animal-focused measures. A narrative review of the literature was conducted to bring together recent studies examining welfare assessment methods in zoo animals. A summary of these methods is provided, with advantages and limitations of the approaches presented. We then highlight practical considerations with respect to implementation of these tools into practice, for example scoring schemes, weighting of criteria, and innate animal factors for consideration. It is concluded that there would be value in standardizing guidelines for development of welfare assessment tools since zoo accreditation bodies rarely prescribe these. There is also a need to develop taxon or species-specific assessment tools to complement more generic processes and more directly inform welfare management.

Natural Habitat Design for Zoo-Housed Elasmobranch and Teleost Fish Species Improves Behavioural Repertoire and Space Use in a Visitor Facing Exhibit.

This study investigated the behaviour of two Elasmobranch species; Southern fiddler ray (Trygonorrhina dumerilii, n = 1) and Port Jackson shark (Heterodontus portusjacksoni, n = 4) and two teleost species; moonlighter (Tilodon sexfasciatus, n = 1) and banded morwong (Cheilodactylus spectabilis, n = 1) living within a single enclosure. For this study, two treatments were compared, the original enclosure design, and then after the enclosure had been renovated to more closely represent the species natural habitats, with a raised front viewing glass to prevent visitor interaction. Behaviours such as resting, swimming and abnormal behaviours such as surface and perimeter swimming (elasmobranchs only) were recorded as well as location within the enclosure, for 10 days pre and 10 days post renovation. The Port Jackson sharks significantly reduced the performance of abnormal behaviours after renovation, and significantly increased the time spent near the exhibit front. The Southern fiddler ray increased resting post renovation, while the teleost species also spent more time near the exhibit front. Although a small sample size was used, the results suggest that a more naturalistic environment with multiple micro-habitats and effective visitor barriers allows for a greater proportion of the day spent exhibiting natural behaviours, greater space use and reduced stereotypes.

Identification of Animal-Based Welfare Indicators in Captive Reptiles: A Delphi Consultation Survey.

There is an increasing focus on evidence-based welfare assessment by animal care staff in zoos, along with a strong interest in animal welfare by the zoo-visiting public, to the extent that this can influence their choice of institutions to visit. Regulatory oversight of animal welfare standards continues to strengthen across many jurisdictions. Zoos are increasingly formalizing their practices with the development and refinement of evidence-based welfare assessment tools. There has been a drive for welfare assessment tools to comprise both resource-based and animal-based measures. However, animal-based indicators are not always well characterized, in terms of their nature and whether they infer a positive or negative affective state. This is especially so for reptiles, which are often considered behaviorally inexpressive and are under-researched. In this study, a Delphi consultation approach was used to gather expert opinion on the suitability of potential animal-based indicators of welfare for inclusion in a welfare assessment tool across four families of reptiles: Agamidae, Chelidae, Pythonidae, and Testudinidae. Two rounds of online surveys were conducted eliciting responses from a global group of professionals who work with reptiles. In the first survey, respondents were provided with an author-derived list of potential animal-based indicators for consideration of their validity and practicality as welfare indicators. The indicators were refined for the second survey including only those indicators that were considered valid or practical on the first survey (≥4 on a 5-point Likert scale), and that achieved ≥70% consensus amongst experts. In the second survey, respondents were asked to re-evaluate the reliability and practicality of the indicators and to rank them on these facets. Eight to ten assessment indicators for each family of reptiles were identified from Survey 2. These indicators were often health related, for example, presence of oculo-nasal discharge or wounds. However, some true behavioral indicators were identified, such as showing species-specific interest and alertness. These indicators should now be incorporated into taxon-tailored welfare assessment tools for trial and validation in captive reptile populations. This study provides a next step towards developing reptile-specific animal welfare assessment tools for these often-overlooked animals.

Cognitive Enrichment in Practice: A Survey of Factors Affecting Its Implementation in Zoos Globally.

Information on the practical use of cognitive enrichment in zoos is scarce. This survey aimed to identify where cognitive enrichment is being used while identifying factors that may limit its implementation and success. Distributed in eight languages to increase global range, responses to this survey (n = 177) show that while agreement on what constitutes cognitive enrichment is poor, it is universally perceived as very important for animal welfare. Carnivores were the animal group most reported to receive cognitive enrichment (76.3%), while amphibians and fish the least (16.9%). All animal groups had a percentage of participants indicating animal groups in their facility were not receiving cognitive enrichment when they believe that they should (29.4-44.6%). On average, factors relating to time and finance were rated most highly in terms of effect on cognitive enrichment use, and keeper interest was the highest rated for effect on success. Results of this study indicate that cognitive enrichment is perceived as important. However, placing the responsibility of its development and implementation on animal keepers who are already time-poor may be impeding its use. A commitment to incorporating cognitive enrichment into routine husbandry, including financial support and investment into staff is needed from zoos to ensure continued improvement to captive animal welfare.

Emergency Response to Australia's Black Summer 2019-2020: The Role of a Zoo-Based Conservation Organisation in Wildlife Triage, Rescue, and Resilience for the Future.

Modern zoos are increasingly taking a leading role in emergency management and wildlife recovery. In the face of climate change and the predicted increase in frequency and magnitude of catastrophic events, zoos provide specialised expertise to assist wildlife welfare and endangered species recovery. In the 2019-2020 Australian bushfire season, now called Australia's Black Summer, a state government-directed response was developed, assembling specialised individuals and organisations from government, non-government organisations, research institutions, and others. Here, we detail the role of Zoos Victoria staff in wildlife triage and welfare, threatened species evacuation and recovery, media and communications, and fundraising during and after the fires. We share strategies for future resilience, readiness, and the ability to mobilise quickly in catastrophic events. The development of triage protocols, emergency response kits, emergency enclosures, and expanded and new captive breeding programs is underway, as are programs for care of staff mental health and nature-based community healing for people directly affected by the fires. We hope this account of our response to one of the greatest recent threats to Australia's biodiversity, and steps to prepare for the future will assist other zoos and wildlife organisations around the world in preparations to help wildlife before, during, and after catastrophic events.

Visitor Attitudes Toward Little Penguins (Eudyptula minor) at Two Australian Zoos.

This study identified and compared the attitudes of visitors toward zoo-housed little penguins, their enclosure and visitor experience that may influence the way visitors behave toward little penguins at two Australian zoos. Visitor attitudes were assessed using an anonymous questionnaire, targeting visitor beliefs, and experiences, where visitors were randomly approached at the penguin exhibit after they had finished viewing the penguins. Visitors were given two options to complete the questionnaire, on an iPad during their zoo visit or online (URL sent via email) after their zoo visit. A total of 638 participants (495 at Melbourne Zoo and 143 at Taronga Zoo) completed the questionnaire, 42% were completed onsite during their zoo visit and 58% were completed online after their zoo visit. Most participants were living in Australia, non-zoo members, female, previously or currently owned a pet, aged between 26 and 35 years and had a University degree. Results showed that the attitude dimensions of visitors were consistent between the two zoos which indicates that these measures of attitudes were stable over time and location. Overall, visitors at both zoos had positive attitudes toward little penguins, penguin welfare, the enclosure, and visitor experience. However, whether these positive attitudes and positive visitor experience influenced the way visitors behaved toward the penguins remains unclear. There were some differences in visitor attitudes toward the perceived "aggressiveness" and "timidness" of little penguins, "negative penguin welfare", "experience with the penguins", "learning", "visual barriers" and the way visitors rated their overall experience at the penguin enclosure. While the reasons for the differences in visitor attitudes and visitor experience between the zoos were not clear, some factors such as penguin behavior and enclosure design, may have been attributable to these differences. Also, a relationship was found between visitor attitudes and how visitors rated the welfare of penguins, the enclosure and visitor experience at the enclosure; more positive visitor attitudes were associated with higher ratings of penguin welfare, the enclosure and visitor experience. The practical implications of these results for zoos is unclear because the differences in visitor attitudes were numerically small. This requires further comparisons between zoos or enclosures that are more markedly different than the penguin enclosures in the present study and further research on how visitors assess zoo animals, enclosures and visitor experience.

Effect of Covering a Visitor Viewing Area Window on the Behaviour of Zoo-Housed Little Penguins (Eudyptula minor).

Studies on the effects of visitors on zoo animals have shown mixed findings and as a result, the manner in which visitors affect zoo animals remains unclear for many species, including a rarely studied taxa such as penguins. Penguins are a common zoo-housed species and have been shown to display huddling, vigilance and avoidance towards zoo visitors which can be indicative of fear. Here, we examined the effects of covering one visitor viewing area window, out of four, on little penguin (Eudyptula minor) behaviours that may be indicative of fear. Two treatments were randomly imposed on different days: (1) The main visitor viewing area window, where most visitor-penguin interactions occurred, was uncovered ('Main window uncovered') and (2) The main visitor viewing area window was covered ('Main window covered'). Penguin numbers and behaviour were recorded near the main visitor viewing area window and the three other visitor viewing area windows, as well as one area not visible to visitors ('Corner' area). Furthermore, visitor numbers and visitor behaviour were recorded at all four visitor viewing area windows. Covering the main visitor viewing area window reduced the proportion of visitors present at this window by about 85% (p < 0.001) and reduced potentially threatening visitor behaviours at this window such as tactile contact with the window, loud vocalisations and sudden movement (p < 0.05). When the main visitor viewing area window was covered, the proportion of penguins present increased by about 25% (p < 0.05), the proportion of visible penguins preening in the water increased by about 180% (p < 0.05) and the proportion of visible penguins vigilant decreased by about 70% (p < 0.05) in the area near this main window. A preference for the Corner area was also found whereby 59% and 49% of penguins were present in this area when the main window was uncovered and covered, respectively. These results provide limited evidence that the little penguins in this exhibit showed an aversion to the area near the main visitor viewing area window when it was uncovered based on the increased avoidance and vigilance and decreased preening in the water in this area. This suggests visitors may be fear-provoking for these little penguins. However, it is unclear whether visual contact with visitors per se or other aspects of visitor contact, such as visitor-induced sounds and vibrations, were responsible for this apparent aversion when this window was uncovered.

The Effect of Regulating Zoo Visitor-Penguin Interactions on Zoo Visitor Attitudes.

Understanding visitor attitudes toward zoo animals can inform the way zoos manage visitor-animal interactions by identifying the factors that may influence visitors and the way visitors interact with animals. Consequently, we investigated the relationship between visitor attitudes and penguin behavior and the effects of regulating visitor-penguin interactions on visitor attitudes and experience. Visitor attitudes toward little penguins (Eudyptula minor), their welfare, enclosure, visitor effects, enclosure manipulations and visitor experience at an Australian zoo were assessed. A 2 × 2 fully randomized factorial design was used to examine potential factors that may influence visitor attitudes: (1) Viewing proximity of visitors to the enclosure: "Normal viewing distance" and "Increased viewing distance" (using a physical barrier set up 2 m from the enclosure) and (2) Intensity of visitor behaviors: "Unregulated visitor behavior" and "Regulated visitor behavior" (using signage and researcher in zoo uniform). Visitor attitudes were assessed using an anonymous attitude questionnaire. Visitors were approached after they had finished viewing the penguins and were given two options to complete the questionnaire, either on an iPad on site during their zoo visit or online (URL sent via email) after their zoo visit. A total of 495 surveys (48% during zoo visit, 52% after zoo visit) were completed. Majority of respondents were non-zoo members, females and aged between 26 and 35 years old. Results revealed a significant relationship (p < 0.05) between little penguin behavior and visitor attitudes where the more visible, active and close penguins were to the visitor viewing area, the more positive several visitor attitude scales were. In contrast, there were only a few treatment effects of regulating visitor viewing proximity and behavior on visitor attitudes in which attitudes toward "Positive penguin characteristics" (p = 0.024), "Neutral visitor effects" (p = 0.0023) and "Physical barriers" (p = 0.013) were affected. This suggests that physical barriers and/or signage are factors that influence visitor attitudes. However, it is unclear if the treatment effects influenced visitor attitudes directly, or if it was the changes in penguin behavior as a consequence of the treatments that were associated with visitor attitudes. These findings have increased our understanding of the multifaceted nature of visitor attitudes and have identified some influencing factors on attitudes that can be used to inform the way zoos manage visitor-penguin interactions, but clearly further research is required.

The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare.

Achieving and maintaining high standards of animal welfare is critical to the success of a modern zoo. Research has shown that an animal's welfare is highly dependent on how various individual animal factors (e.g., species traits, genetics, temperament and previous experience) interact with environmental features (e.g., social grouping, enclosure design and sensory environment). One prominent feature of the zoo environment is the presence of visitors. Visitor contact can be unpredictable and intense, particularly in terms of auditory and visual interaction. Depending on an animal's perception of this interaction, visitors can have either negative, neutral or positive impacts on zoo animal behaviour and welfare. This paper reviews the literature on the implications and potential opportunities of human-zoo animal interactions on animal behaviour and welfare, with the aim of stimulating interest, understanding and exploration of this important subject. The literature to date presents a mixed range of findings on the topic. It is possible this variation in the responses of zoo animals to visitors may be due to species-specific differences, the nature and intensity of the visitor interactions, enclosure design, and individual animal characteristics. Analysing these studies and better understanding animal preferences and motivations can provide insight into what animals find negatively and positively reinforcing in terms of visitor contact in a specific zoo setting. This understanding can then be applied to either safeguard welfare in cases where visitors can have a negative impact, or, conversely, it can be applied to highlight opportunities to encourage animal-visitor interaction in situations where animals experience positive emotions associated with visitor interaction.

Effects of Regulating Visitor Viewing Proximity and the Intensity of Visitor Behaviour on Little Penguin (Eudyptula minor) Behaviour and Welfare.

We examined the effects of regulating the viewing proximity of visitors and the intensity of visitor behaviour on behaviours indicative of fear and stress physiology of 15 zoo-housed little penguins (Eudyptula minor). A 2 × 2 factorial fully randomised design was used to examine the effects of regulating: 1) the viewing proximity of visitors to enclosure, 'normal viewing distance' and 'increased viewing distance' (using a physical barrier set up 2 m away from the enclosure), and 2) the intensity of visitor behaviour, 'unregulated visitor behaviour' and 'regulated visitor behaviour' (using signage and uniformed personnel). In addition, a treatment consisting of closing the enclosure to visitors was included. Penguin behaviour, visitor numbers and visitor behaviour were recorded by CCTV video recordings and direct observations, respectively. Penguin faecal glucocorticoid metabolites were also analysed as a measure of stress physiology. We found that increased viewing distance reduced (p < 0.05) all visitor behaviours except for loud vocalisations and tactile contact with penguins. However, there were no direct effects of signage and uniformed personnel on visitor behaviour (p > 0.05). As the regulation of viewing proximity increased from a closed exhibit to an open exhibit with increased viewing distance, and then to an open exhibit with normal viewing distance, this increased the proportion of penguins huddling (p = 0.0011), vigilant (p = 0.0060) and retreating (p = 0.00013), and decreased the proportion of penguins within 1 m of the visitor viewing area (p = 0.00066), surface swimming (p = 0.00091) and preening in the water (p = 0.042). There were also limited effects of regulating visitor behaviour on penguin behaviour. No treatment effects were found on faecal glucocorticoid metabolites (p > 0.05). These results indicate that regulating visitor viewing proximity affects penguin behaviours indicative of fear and visitor behaviour. This suggests that close visitor contact can be fear-provoking for little penguins but increasing the distance between visitors and penguins can reduce fear responses of penguins by regulating both viewing proximity and visitor behaviour. However, it is unclear whether these changes in penguin behaviour are due to the increased separation between visitors and penguins and/or specific visitor behaviours associated with close viewing proximity to the enclosure, such as leaning over the enclosure or tactile contact with the pool, which are impeded when visitors are further away.

An Animal Welfare Risk Assessment Process for Zoos.

There is a growing interest and need for zoos to develop and implement welfare assessment tools that are practical to use and provide meaningful results that can inform management decisions. This paper presents a process that was developed to support this type of evidence-based management in zoo animal welfare. The process is configured to facilitate institutional risk assessment, using an adapted version of the Five Domains Model for animal welfare assessment. It is designed to systematically analyse information gathered from zoo personnel in order to highlight areas of welfare risk, as well as areas that are performing well and areas requiring further investigation. A trial was conducted on three zoos over three years. Results of the trial suggest the process developed is practical and effective in identifying areas of welfare risk in a wide range of species in a zoo setting. It represents a further step towards achieving high-level animal welfare in zoos by integrating animal welfare as an institutional priority. The more zoos that employ such strategies, the greater the ability of the sector to advance the welfare of the animals in their care.

Impacts of visitor number on Kangaroos housed in free-range exhibits.

Free range exhibits are becoming increasingly popular in zoos as a means to enhance interaction between visitors and animals. However very little research exists on the impacts of visitors on animal behaviour and stress in free range exhibits. We investigated the effects of visitor number on the behaviour and stress physiology of Kangaroo Island (KI) Kangaroos, Macropus fuliginosus fuliginosus, and Red Kangaroos, Macropus rufus, housed in two free range exhibits in Australian zoos. Behavioural observations were conducted on individual kangaroos at each site using instantaneous scan sampling to record activity (e.g., vigilance, foraging, resting) and distance from the visitor pathway. Individually identifiable faecal samples were collected at the end of each study day and analysed for faecal glucocorticoid metabolite (FGM) concentration. When visitor number increased, both KI Kangaroos and Red Kangaroos increased the time spent engaged in visitor-directed vigilance and KI Kangaroos also increased the time spent engaged in locomotion and decreased the time spent resting. There was no effect of visitor number on the distance kangaroos positioned themselves from the visitor pathway or FGM concentration in either species. While there are limitations in interpreting these results in terms of fear of visitors, there was no evidence of adverse effects animal welfare in these study groups based on avoidance behaviour or stress physiology under the range of visitor numbers that we studied.