Zoo Animal Welfare Research Articles

Stress produces negative judgement bias in cuttlefish.

Judgement bias tasks (JBTs) are used to assess the emotional state and welfare of animals in zoos, farms and laboratories, based on the interpretation of an ambiguous or intermediate cue. Animals in positive affective states are more likely to interpret the ambiguous cue positively, whereas animals experiencing negative affect are more likely to interpret ambiguous cues pessimistically. Here, we developed a modified JBT assay for the stumpy-spined cuttlefish, Sepia bandensis, to determine whether cuttlefish exhibit negative affective states resulting from external stressors. Positive and neutral visual cues were presented twice daily until animals learned to associate food with the reinforced visual cue. After training, one treatment group was exposed to combined exposure and handling stress produced by 6 days of impoverished housing and simulated net capture. Our control group received no stress experience. In test trials performed after the stress experience, stressed animals showed higher latencies to approach ambiguous cues, spent significantly less time in rooms with ambiguous cues once they entered, and were less likely to enter first into the ambiguous cue-paired room compared with controls. These behaviours suggest that stress induces pessimistic judgement bias in cuttlefish, the first indication of this capacity in cephalopods.

The Effects of Enrichment on Zoo-Housed Scarlet Ibis Behavior.

Good zoo animal welfare is commonly promoted with environmental enrichment; however, some species are less likely to be offered enrichment than others. This study tested the effect of enrichment on a group of scarlet ibises from Zoomarine Algarve, Portugal. The study consisted of a first baseline condition, followed by four types of enrichment displays with individual presentations, a post-enrichment condition, and a post-enrichment with all enrichment types presented simultaneously. The enrichment types chosen were physical, with a tidal simulation in the lakes of the enclosure; nutritional, presenting mussels in a plastic mesh tube; sensory, by playing scarlet ibises calls; and tactile, with brushes through the habitat. The data collection was performed for 21 days between January and March 2021, 3 times a day, using scan sampling and instantaneous time sampling every 2 min. The comparison between conditions revealed that most behaviors showed similarity between the baseline and post-enrichment conditions, suggesting that after removing the enrichment, the behaviors returned to their initial baseline. It was also found that each enrichment influenced different types of behaviors and these behaviors also changed depending on the time of day. Exploratory behavior was only associated with the presence of enrichment, and vocalizations were only heard after the sensory enrichment was performed. This study demonstrates that the use of physical and tactile enrichments increased activity and decreased stationary behaviors in this group of ibises and may be used to improve their lives in zoological contexts if included in the housing and husbandry protocols.

Parasitological examination results of zoo animals in Germany between 2012 and 2022

Parasitic infections in zoo animals are a critical concern for both animal health and management. The aim of this study was to assess the occurrence of endo- and ectoparasites among zoo animals in Germany. A retrospective analysis of the submitted samples of a diverse range of zoo animals (5768) from a ten-year period (2012–2022) was conducted. Overall, 31.1% of those samples tested positive for at least one parasite. In the examined samples, helminths (28.4%) were found more often than protozoans (10.3%) or ectoparasites (0.8%). Among the various animal groups the following parasites were found most commonly: Artiodactyla: Coccidia (34.6%), Strongylida (23.4%); Perissodactyla: Strongylida (19.3%), Ascaridida (12.0%); Carnivora: Ascaridida (16.6%), Coccidia (8.1%); Rodentia: Oxyurida (18.2%), Coccidia (10.5%); Marsupialia: Coccidia (9.4%), Oxyurida (5.9%); Primates: Trichuris spp. (9.7%), Oxyurida (2.2%); Aves: Capillaria (7.8%), Ascaridida (7.6%); Reptilia, Amphibia, Insecta: Oxyurida (18.7%); Pisces: Ciliates (6.2%). Furthermore, potentially zoonotic parasites were identified, including Toxoplasma gondii (0.1%), Cryptosporidium sp. (0.1%). By examining the occurrence of specific parasites, these findings demonstrate the importance of parasites in the context of zoo animal health. They also highlight the need for effective strategies to control parasite burden to improve the overall welfare of zoo animals.

Advancing zoo animal welfare through data science: scaling up continuous improvement efforts.

Advancing zoo animal welfare through data science: scaling up continuous improvement efforts.

Quality-of-Life Assessments in Zoo Animals: Not Just for the Aged and Charismatic.

Zoos should aim to provide all of their animals with a good quality of life (QoL) throughout all life stages. In parallel with the evolution of QoL assessment questionnaires and tools in human and domestic animal settings, in recent times, some individual zoos and zoo industry associations have incorporated such instruments into their animal management practices. This has been conducted predominantly to inform, monitor, and document end-of-life decision-making for large, charismatic mammals. There is scope to expand the use of these tools to improve their utility, validity, reliability, and value to an animal welfare program. Assessment of QoL is a complex task given that the notion being measured is abstract and self-determined, and the design and purpose of the tools to do this require careful consideration. This review explores the QoL concept as it applies to animals, the assessment indications and methodologies relevant to a zoo setting, and the importance of considering QoL at any life stage across species. An overview of current thinking and the applications and limitations of QoL evaluation of captive wild animals is offered to promote and aid facility practice reviews and to help direct future innovations that leverage concurrent and converging advances in zoo animal welfare science.

Manatees in Zoological Parks throughout the World: History, State, and Welfare.

The order Sirenia comprises several species of manatees and one species of dugong. These popular marine mammals are relatively recent acquisitions to zoological parks throughout the world. As far as we know, there are less than 200 manatees, mostly American, a few African, and ever less Amazonian, currently in zoological parks. American manatees are predominantly found in zoos in Europe, North America, and in some Asian countries, while African ones are present exclusively in Asian zoos. The living conditions of captive manatees differ considerably from zoo to zoo (i.e., numbers, sex ratio, outdoor vs. indoor habitats, complex vs. simple habitats). Most research on manatee behaviour has been relatively recent, and studies on cognition, sociality, and ecology have a significant impact on our perception of manatee needs and management, with wider implications for their welfare. In the wild, manatees demonstrated various cognitive capacities; spatial memory and learning abilities play an important role in their daily life in a complex and dynamic environment. Furthermore, there is evidence that these mammals are more social animals than expected. Individuals show various personality traits on the boldness-shyness continuum and their sociality varies. All those parameters are important in terms of animal welfare. Several behavioural studies showed that standardized enrichment programs benefit and ensure the welfare of captive zoo animals. However, obtaining accurate information on the presence of manatees in zoos, living conditions, management, and consequently welfare remains challenging. This study examines the current knowledge on manatee behaviour and cognition and then discusses different approaches to improving the welfare of this charismatic marine mammal in zoological parks.

The Assessment of Animal Personality and Its Uses for Improving Zoo Animal Welfare

Abstract Animal welfare is central to the three aims of the modern zoo: conservation, research and education. Good welfare depends not only on the management of the captive population as a whole but also on the management and husbandry of individual animals. Zoo keepers are able to reliably assess animal personality traits, and these traits are linked to measures of welfare such as reproductive success, stereotypic behaviour and physiological stress. Assessing animal personality can help to address some of the challenges faced in zoo animal management. A validated personality questionnaire is a valuable tool for zoo professionals, as it can be used to predict reproductive success and the cohesion of social groups. Knowledge of animal personality can help keepers to devise management plans for individuals, and improve keeper safety as well as animal welfare. Aspects of individuals’ behaviour can affect the success of reintroduction programmes, so information about personality can also contribute to ex-situ conservation. Information © The Author 2023

Identifying Essential Elements of Good Giraffe Welfare—Can We Use Knowledge of a Species’ Fundamental Needs to Develop Welfare-Focussed Husbandry?

Measurement of zoo animal welfare states enables improvement to husbandry and management to be evidence-based and implemented according to species’ needs. Theoretical welfare concepts are often discussed, and whilst it is helpful to ensure wide consensus across all stakeholders on what welfare comprises, practical application of such evidence-based information is as equally important. All species housed in zoos will have specific needs that must be met by their housing, husbandry, and care to enable them to thrive. Therefore, this paper examined how to identify key animal care needs and an animal’s responses to them to form a basis for species-specific welfare assessment approaches. There are examples of familiar-to-the-zoo species that still pose challenges regarding delivery of optimal husbandry and management. As such, the identification and evaluation of core concepts of the biology, behaviour, “needs and wants” of these species is required to support validation and refinement of physical, behavioural, and psychological welfare measures. This article evaluated the use of evidence to build capacity in welfare measurement for a familiar zoo-housed species, the giraffe (Giraffa camelopardalis, Linnaeus 1758), by outlining seven key needs and requirements that must be provided in the zoo (“giraffe W-E-L-F-A-R-E” = Warmth, Enrichment, Leaves, Feeding, Alfalfa, Rumination, Exercise). Provision of these inputs, and opportunities for all giraffes in a herd to engage with them, provides the foundation for further welfare assessment to be implemented. Specifically, the validation and measurement of mental states that are more likely to be positive if key behavioural and ecological needs have already been met. This paper advocated for this evidence-based approach to “welfare-focussed husbandry”, with distillation of key information that supports species-relevant care, to be developed for other zoo-housed species as support for their welfare assessment protocols. Such welfare-focussed husbandry is layered on top of the basic animal care requirements of the species in the zoo to ensure all individuals have the best opportunity to attain positive welfare states. In this way, and once validated, foundational welfare assessment can be easily completed by busy animal care staff, capacity is built into zoo operations as all stakeholders are aware of exactly what each species needs, and deeper dive welfare assessment (especially concerning animal mental states) can be targeted more effectively. Further evolution of these seven steps for the giraffe is suggested and extrapolation of this approach, to aid identification of key welfare indicators across all zoo-housed species, is encouraged.

Enrichment and animal age, not biological variables, predict positive welfare indicators in zoo-housed carnivores

The development of evidence-based zoo animal welfare science and the use of the 'five domains' have inspired zoos to increase animal welfare, particularly recognising positive welfare states. We tested whether natural biology (number of habitats, latitudinal range, sociality, body weight) or husbandry variables (mean age of group, group size and presence of extra enrichment) predict rates of positive welfare indicators (activity, play and engagement with the environment) in the Order Carnivora from collecting data from previously published articles. For each behaviour, species (n = 23) medians were analysed using phylogenetically informed mixed-model regression. Activity data were from 136 animals (n = 23 species), environmental interaction from 55 animals (n = 15 species) and play from 27 animals (n = 7 species). Biological variables did not predict rates of behaviour at a species or an individual animal level, but husbandry variables did. At an individual level, activity and play decreased in older animals. Activity and interaction with environment also increased with additional enrichment. This study is the first to quantify positive behaviours performed by zoo housed Carnivora and shows that they display indicators of positive welfare, if appropriate husbandry including environmental enrichment is provided.

The Role of Preventative Medicine Programs in Animal Welfare and Wellbeing in Zoological Institutions.

The overarching goal of a preventative medicine program is to minimize the chances of health problems developing and to maximize the chances of detecting health problems early, in a manner that best benefits the animals and the organization. The traditional paradigms of animal welfare, stemming from the five freedoms and being progressively fleshed out to five domains, the 24/7 approach and so forth do not apply perfectly to zoological collections and less so to animals undergoing veterinary treatments. The physiology and behaviour of animals undergoing veterinary treatments, including therapeutic, quarantine and preventative medicine, are derailed from their normal states and their choices and comfort are de facto limited. A paradigm separating animal wellbeing from animal welfare is necessary to instil clarity of thought and to guide actions in regard to the welfare of animals under human care. Using such a model, preventative medicine programs emerge as a cornerstone of zoo and aquarium animal welfare, all the more if it incorporates modern veterinary and husbandry techniques, including operant conditioning.

Zoo Animal Welfare Assessment: Where Do We Stand?

Zoological institutions, such as zoos and aquariums, have made animal welfare a top priority, as it is not only a moral obligation but also crucial for fulfilling their roles in education and conservation. There is a need for science-based tools to assess and monitor animal welfare in these settings. However, assessing the welfare of zoo animals is challenging due to the diversity of species and lack of knowledge on their specific needs. This review aims to discuss the advantages and disadvantages of existing methodologies for assessing zoo animal welfare through: (1) A critical analysis of the main approaches to zoo animal welfare assessment; (2) A description of the most relevant animal-based welfare indicators for zoo animals with a particular focus on behavioural and physiological indicators; and (3) An identification of areas that require further research.

Integrating Individual Animal and Population Welfare in Zoos and Aquariums.

Over the last 50 years, animal welfare science has advanced dramatically, especially in zoos and aquariums. A shifting focus from population-level welfare parameters such as reproductive success and longevity (macroscopic, big-picture concepts) to the subjective experience of individual animals (microscopic, focused concepts) has led to more effective animal welfare assessments and improvements in animal welfare. The interplay between individual animal and population welfare for captive animals is critical to the way zoos and aquariums operate to realize their welfare and conservation missions, especially when these missions conflict with one another. In this report, we explore the intersection of individual animal and population welfare in zoos and aquariums and how these two concepts may support one another or be in conflict.

Individual personality predicts social network assemblages in a colonial bird

Animal personalities manifest as consistent individual differences in the performance of specific behavioural expressions. Personality research has implications for zoo animal welfare, as it can further our understanding of how captive individuals may differ in their resource use and provide insight into improving individual and group social health. For group living species, personality may enable assortment based on similar behaviour and influence an individual’s interactions with conspecifics (e.g. social support). This research aimed to document how personality traits (aggressive, exploratory, submissive) influenced the social network structure of highly social animals in a captive environment. Data were collected from separate flocks of captive Caribbean (Phoenicopterus ruber) and Chilean flamingos (Phoenicopterus chilensis) to identify relationships between birds and examine opportunities for social support. The flocks associated non-randomly, and in both cases, personality was a substantial predictor of network structure. Personality also predicted key elements of Caribbean flamingo social role (degree, betweenness and average association strength) conflict outcome, and propensity to provide social support, however these patterns were not replicated within the Chilean flamingo network. While both species appear to assort by personality, the broader relationship between personality and social role may vary depending on species and context.

Don't use it? Don't lose it! Whyactive use is not required for stimuli, resources or "enrichments" to have welfare value.

Current frameworks for designing and evaluating good enclosures and "enrichments" typically focus on animals' active interactions with these features. This has undoubtedly improved the welfare of zoo-housed animals over the last 30 years or more. However, literature reviews from this same period identify persistent gaps in how such frameworks are applied: experiences and behaviors that do not rely on active interaction with stimuli or resources are largely ignored, when evaluating the welfare value of enclosures andenrichments within them.Here, we review research evidence demonstrating that active interaction is not always a reliable measure of welfarevalue, showing that items that elicit little or no interaction can nevertheless still reduce stress and improve well-being. This evidence largely comes from research on humans, lab animals and farm animals, but also from some zoo studies too.We then investigate why. We review psychology and ethology literatures to show that such welfare benefits can arise from five, non-mutually exclusive, processes or mechanisms that are well-understood in humans and domestic animals: (1) some motivations are sated quickly by interaction with resources, yet still have large welfare benefits; (2) active interaction may just be a way to achieve a goal or solve a problem, without being beneficial for welfare in itself; (3) having opportunities for choice and control may be inherently beneficial, even when not acted on; (4) some enclosure features meet social needs for structure, landmarks, and blocked sightlines; and (5) some stimuli may be preferred because they signaled good environments to an animal's ancestors. We use this information to identify improved ways of enhancing and assessing zoo animal welfare. Incorporating these concepts should expand the scope of behaviors and subjective experiences that are targeted, to now include those that involve little active interaction and yet still are important for good welfare.

Access to Multiple Habitats Improves Welfare: A Case Study of Two Zoo-Housed Black Bears (Ursus americanus)

Using various forms of enrichment, animal care specialists encourage species-specific behaviors and discourage stereotypic behaviors. Within the zoo community, bears (Ursids spp.) are commonly housed, yet are prone to exhibiting stress-related behaviors. Here, we assess the effect of access to multiple habitats, including areas of off guest view, on the welfare of two American black bears (U. americanus) housed at the North Carolina Zoo. In this study, we looked at two behaviors, pacing and foraging to represent negative and positive welfare indicators. We performed logistic regressions to model the effect of access on these behaviors. Because having an animal visible to guests is important to consider when creating management plans, we also explored the effect of access on the bears’ visibility. We found that full access reduced the likelihood of pacing by an average of 13% and increased the likelihood of foraging by an average of 5%. Access to multiple areas reduced the probability of visibility by 57% for one individual but did not impact visibility of the other bear. This case study suggests the value of access to zoo animal welfare and should incite future research aimed at exploring the effects of access on various behavioral outcomes.

Exploration of cultural norms and behavioural beliefs about zoo animal behaviour, welfare, ethics and husbandry practices in a sample of the international zoo community.

Beliefs influence the intentions of people to behave in certain ways towards animals. This study presents survey responses from 237 people working in zoos in China and Europe and describes their demographic characteristics. It explores their beliefs about zoo animal behaviour, welfare and ethical issues, and zoo practices, using a survey methodology. These beliefs may be influenced by individual demographic or cultural factors such as age, genderand region of employment, as well as experiential or situative 'norms' within the work environment. Beliefs were significantly influenced by the region of employment with Chinese respondents beliefs being significantly different to beliefs from respondents in the United Kingdom or the rest of Europe. Hierarchical cluster analysis of the survey generated clusters of people from both regions who indicated positive beliefs about zoo animal welfare as well as clu sters indicating a lack of understanding of some zoo animal welfare issues. In addition, a cluster suggesting cognitive dissonance between beliefs about animals welfare and zoo practices was generated from Chinese responses. Factor analysis identified that prioritisation of in-situ conservation within good animal welfare was a key feature in Chinese respondents, whereas European beliefs prioritising in-situ conservation were distinct from those on supporting good animal welfare. This paper identifies similarities and differences in beliefs about zoo animal welfare and zoo husbandry practices between Europe and China, and discusses the underlying norms and values that these beliefs may reflect.

Ackonc-AWA: A multi-species animal welfare assessment protocol for wild animals under human care to overcome the use of generic welfare checklists.

Maintaining a high level of animal welfare is essential in zoos, sanctuaries and aquaria for ethical, legislative and functional reasons. Therefore, it is necessary to have welfare assessment protocols that can be incorporated into daily management programs. Currently, there are different approaches to assessing animal welfare in zoos. Those that can be applied to multiple species consist of checklists or qualitative assessments, with limitations, especially regarding the lack of guidance in the selection and interpretation of indicators. Validated protocols also exist, but they are for very few wild species. This study aimed to develop, test in the field, and describe an animal welfare assessment protocol for wild animals under human care, that can be applied to multiple species, intended to overcome the use of generic welfare checklists and offer an alternative to challenging and time consuming species-specific tools. The development process consisted of the elaboration of a protocol, substantiated by published literature on zoo animal welfare and multidisciplinary focus group work, and its on-field feasibility test. This was performed on 14 species of different taxa housed in an Argentinian zoo. The protocol was structured in two forms: an initial form to serve as scan using various animal-based (ABM), resource-based (RBM), and management-based measurements (MBM), and a follow-up form using exclusively ABM. The protocol also included a user's manual with information about preliminary preparation, equipment required, steps from arrival until completion, and details on how to assess each indicator. The scoring method consisted in rating each indicator on a 3-point scale. 23 ABM, 19 RBM, and three MBM were tested and selected to integrate Ackonc-AWA, a multidimensional protocol covering the five animal welfare domains and applicable to multiple species. This protocol was entirely developed in Spanish and can be applied noninvasively and at a low cost, which constitute features of high relevance for Latin America. Further applications of the described welfare assessment tool in other species and different institutional contexts will reinforce the validation of the proposed measurements and allow the systematic and routine evaluation of animal welfare in zoos.

An Improvement in Enclosure Design Can Positively Impact Welfare, Reduce Aggressiveness and Stabilise Hierarchy in Captive Galapagos Giant Tortoises

The interest in the welfare of zoo animals, from both the public and the scientific community, has long been biased towards mammals. However, growing evidence of the complex behavioural repertoires of less charismatic animals, such as reptiles, reveals the necessity to better comply with their welfare needs in captivity. Here, we present the effects of an enclosure change towards a more natural habitat in captive Galapagos tortoises (Chelonoidis spp.) held at ZSL London Zoo. Using behavioural observations, we found that the tortoises habituated to their new enclosure in six days. This represents the first quantification of habituation latency to a new enclosure in a reptile model to our knowledge—which is important information to adapt policies governing animal moves. The tortoises expressed time budgets more similar to those of wild individuals after their transition to the new enclosure. Interestingly, the hierarchy between the individuals was inverted and more stable after this change in environment. The tortoises interacted less often, which led to a decrease in the frequency of agonistic encounters. We also found that higher ambient sound volume was associated with increased likelihood of interactions turning into fights. Taken together, our results demonstrate the potential of appropriate enclosure design to improve reptile welfare.

An Approach to Assessing Zoo Animal Welfare in a Rarely Studied Species, the Common Cusimanse Crossarchus obscurus

Objective welfare assessments play a fundamental role in ensuring that positive welfare is achieved and maintained for animals in captivity. The Animal Welfare Assessment Grid (AWAG), a welfare assessment tool, has been validated for use with a variety of both domestic and exotic species. It combines both resource- and animal-based measures but relies heavily on knowledge of the species to effectively assess welfare. Many zoo species are understudied in the wild due to their cryptic nature or habitat choice; therefore, the published literature needs to be supported with captive behavioural observations and zoo records. Here we adapted previously published AWAG templates to assess the welfare of Crossarchus obscurus. A total of 21 factors were identified, and the final template was used to retrospectively score the welfare of two male and two female C. obscurus at Marwell Zoo, UK, validating the use of this process for preparing a welfare assessment for a species where the published literature is scarce.

Behavioral Changes of Brown Bears (Ursus arctos) during COVID-19 Zoo Closures and Further Reopening to the Public

Visitor effect studies have been of keen interest for decades, but there have been only anecdotal opportunities to investigate the impact of the prolonged absence of visitors on animal welfare in zoos. In some zoos, bears are actively involved in animal–visitors interaction through begging, which gives them some degree of control over gaining food rewards throughout the day when visitors are present. Prolonged visitor absence may, therefore, represent a loss of control and have a negative impact on the bears’ welfare. In this study, we investigate the behavior of four brown bears (Ursus arctos) in three zoos to see how the animals’ behavior changed depending on the presence and absence of the public during zoo closures in 2020 related to the COVID-19 pandemic. The bears’ behavior was assessed using activity budget analysis and novel object tests. The results showed that the bears behavior varied between facilities and that there was no effect of visitor presence for the individuals who had access to indoor holding space. The results of the study are discussed in terms of choice and control and their impact on the wellbeing of bears in zoos.