Edinburgh Zoo Research Articles

The Royal Zoological Society of Scotland's Approach to Assessing and Promoting Animal Welfare in Collaboration with Universities.

Good zoos have four aims-to conserve species, educate the public, engage in research, and provide recreation-all of which can only be achieved when underpinned by high animal welfare standards. In this paper, we share the approach that The Royal Zoological Society of Scotland's (RZSS) Edinburgh Zoo and Highland Wildlife Park take to animal welfare. We highlight the role that animal welfare research, in collaboration with universities, has had in enabling the zoo to take an evidence-based approach to welfare and to put findings into practice. We share the collaborative process through which we developed and piloted the current animal welfare assessment tools, how they were validated, and how they were tested for reliability as part of a long-term collaboration between the Royal Zoological Society of Scotland and the University of Stirling: (1) the RZSS Welfare Assessment Tool, a 50-question animal welfare assessment adapted from the British and Irish Association of Zoos and Aquariums (BIAZA) Toolkit; and (2) the Stirling Toolkit, a package of evidence-based resources for behavioural-data collection. Our aim is to facilitate standardised, evidence-based approaches to assessing animal welfare which, when finalised, can be used collaboratively across zoos.

Do mixed-species groups of capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) synchronize their behaviour?

In the wild, coordinated behaviour across group members is essential for maintaining spatial coherence, with potential implications for individual fitness. Such coordination often leads to behavioural synchrony (performing the same behaviour at the same time). Tufted capuchins (Sapajus apella) and squirrel monkeys (Saimiri sciureus) are known to form mixed-species groups (MSGs), travelling and foraging together. Yet, it is unclear if it is necessary to synchronize behaviours in captivity when ecological pressures are minimal compared to the wild. We investigated the extent to which two MSGs of capuchins (N = 35) and squirrel monkeys (N = 26) synchronized their behaviour with conspecifics and heterospecifics at the Living Links to Human Evolution Research Centre, RZSS, Edinburgh Zoo, UK. Group activities were sampled by instantaneous scans of all visible individuals. Scans (n = 180) were analysed for five most frequently observed behaviours. Intraspecies synchrony was calculated using Simpson's Diversity Index, and interspecies synchrony was measured using cross-correlations. Intraspecific synchrony was significantly greater compared to randomly aggregated data, while cross-correlations indicated interspecific asynchrony. Living together did not lead to interspecific synchrony as may be expected given the coordination and behaviour described in the wild, and shared husbandry in captivity. Overall, our findings highlight differences in the behavioural structure of single- versus MSGs. This article is part of the theme issue 'Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes'.

It’s Virtually Summer, Can the Zoo Come to You? Zoo Summer School Engagement in an Online Setting

Zoological collections are rapidly changing from a place of entertainment to centers of education. Many zoological collections run holiday and weekend clubs with activities aimed at inspiring and enthusing the next generation. The COVID-19 pandemic saw zoological collections across the world closing, leading a need for alternative educational content. Edinburgh Zoo, UK converted their summer school to a virtual provision. This provided a unique opportunity to determine the effectiveness of online zoological education by investigating if engagement levels differ for family groups when education is ‘live’, ‘recorded’ or ‘activity’ based. A total of 235 participants signed up for the Virtual Summer School, which comprised of 46 separate activities. Submissions, comments and polls were coded for content level and activity type. Results show that the overall engagement was higher for the live sessions compared to the recorded content; however, the content level was higher for activities. Content level increased over the week and there was a higher reported nature appreciation at the end of the Virtual Summer School. These findings provided evidence to suggest that online holiday zoo education can engage and inspire and gives insight on how to maximize the engagement and knowledge acquisition when using these online platforms.

A Case Study Exploring the Use of Virtual Reality in the Zoo Context

Virtual Reality (VR) is now a popular tool in education and for engagement with the natural world, but to date little research has investigated its potential in a zoo setting. We aimed to gauge the interest of the visiting public in using VR technology at Royal Zoological Society of Scotland’s (RZSS) Edinburgh Zoo. A VR (n = 12) and a video condition (n = 12), both introducing the lives and conservation concerns of African wild dogs (Lycaon pictus), were used to gain greater insight of the thoughts and perceptions of how individuals evaluated a purpose-built VR experience and to enable comparisons of learning outcomes for both technologies. We used semi-structured interviews; responses were evaluated through thematic analysis and descriptive analysis. Younger participants (aged 13-18 years) emphasized that VR allowed them close and personal access to the animals. Adult participants (aged 19 and above) pointed out the entertainment value of the VR experience while highlighting the potential of its educational aspect; that of enabling visitors to see animals in their natural habitat. While our results require further confirmation due to the limited sample size and restricted circumstances of data collection, we suggest that VR could be usefully introduced as a public education and visitor engagement tool that would benefit the visitors’ learning and overall experience at the zoo.

Exploration of potential triggers for self-directed behaviours and regurgitation and reingestion in zoo-housed chimpanzees

The unique challenges faced by animals living in zoos can lead to the production of anxiety-related behaviours. In this study we aimed to understand what specific factors may cause chimpanzees to display these behaviours. In non-human primates, displacement behaviours, such as self-scratching and yawning, are considered markers of anxiety and stress, and Regurgitation and Reingestion (R/R) is considered an abnormal behaviour with negative consequences for physical health. We examined the possible triggers of R/R, scratching, and yawning in a group of zoo-housed chimpanzees and followed this up with an analysis of long-term data to examine further aspects of R/R behaviour. In the first study we conducted focal observations on 18 adult chimpanzees at Edinburgh Zoo, UK, in addition to all occurrence sampling of visitors using flash photography, screaming and banging on the glass in the exhibit. 158 h of data were analysed and Generalised Linear Mixed Models revealed that yawning was significantly more likely if there was a long period of time since the last feed and when there were moderate numbers of visitors in the zoo. There were trends that yawning was more likely to occur if children screamed and that scratching was more likely to occur if visitors used flash photography. R/R occurred most often within 40 min of a feed, but was not affected by the inter-feed interval preceding that feed, positive or negative social interactions, or visitor numbers or behaviour. As there was no obvious daily trigger for R/R, an analysis of long-term data (2009 to 2015) was conducted to investigate if social or dietary factors affected rates of R/R over a larger timescale. It was found that R/R rates in the months before a significant diet change were not different from R/R rates in the months after, but it was found that R/R rates decreased over the five-year period. Lastly, we found no evidence that the introduction of individuals engaging in R/R lead to resident chimpanzees habitually adopting the behaviour, despite considerable opportunities to observe it. These findings have implications for welfare interventions aimed to reduce R/R and/or anxiety behaviours in captive populations and for the translocation of individuals that are known to engage in R/R between groups.

Chimpanzees with positive welfare are happier, extraverted, and emotionally stable

Facilities housing captive animals are full of staff who, every day, interact with the animals under their care. The expertise and familiarity of staff can be used to monitor animal welfare by means of questionnaires. It was the goal of our study to examine the association between chimpanzee (Pan troglodytes) welfare, happiness, and personality. To these ends we collected two waves of welfare and subjective well-being ratings of 18 chimpanzees housed at the Edinburgh Zoo and one set of ratings of 13 chimpanzees housed at Fundació Mona. Ratings were made on a welfare questionnaire that included 12 items related to stress, psychological stimulation, and behavioural indicators of negative and positive welfare states, and a 4-item subjective well-being questionnaire. In addition, ratings were made on the 54-item Hominoid Personality Questionnaire and an abbreviated version of this scale consisting of 37 antonym pairs. We used generalizability theory to test whether welfare ratings generalized across items, raters, chimpanzees, and time. We then assessed the validity of the welfare and subjective well-being questionnaires by examining their associations with behaviour. Finally, we tested whether the welfare and subjective well-being ratings were associated with personality. Welfare ratings generalized across items, raters, chimpanzees, and time. Principal components analysis and regularized exploratory factor analysis indicated that ten welfare items and all four subjective well-being items formed a single dimension (welfareSWB). LASSO regression found that lower welfareSWB was associated with regurgitation, coprophagy, urophagy, and decreased proximity to nearest neighbour. A linear model that adjusted for age, sex, and facility, indicated that higher Extraversion and lower Neuroticism were related to higher welfareSWB. Welfare ratings were reliable and associated with subjective well-being and personality, demonstrating that staff ratings are a valid and potentially valuable tool for chimpanzee welfare assessment.

A bear’s biography: Hybrid warfare and the more-than-human battlespace

This paper makes an intervention highlighting the animal dimension of military geographies as an overlooked yet illuminating aspect of the hybrid nature of warfare. By bringing animal geographies into dialogue with critical military geographies and with a focus on relational ethics, the processes, performance and consequences of the more-than-human nature of the battlespace are examined through a vignette of Wojtek the bear. Wojtek was a mascot, pet and officially enlisted soldier of the Polish Army in the Second World War who travelled the desert plains, helped to fight at the Battle of Monte Cassino, before being demobbed with his fellow Polish comrades in the UK, eventually ending his civilian days in Edinburgh Zoo. Although a well-known figure Wojtek and his biography have predominately been used as a means to explore the Polish soldiers’ experience of the Second World War with the result that the bear as an animal is absent. This paper, therefore, puts the bear back into his biography in order to acknowledge the role and lived experience of animals in the military. Further, it suggests that exploring the place of animals in the military requires geographers to articulate the hybrid nature of warfare and also to explore the ethico-political relations this produces.

Social Learning in the Real-World: 'Over-Imitation' Occurs in Both Children and Adults Unaware of Participation in an Experiment and Independently of Social Interaction.

The current study avoided the typical laboratory context to determine instead whether over-imitation—the disposition to copy even visibly, causally unnecessary actions—occurs in a real-world context in which participants are unaware of being in an experiment. We disguised a puzzle-box task as an interactive item available to the public within a science engagement zone of Edinburgh Zoo. As a member of the public approached, a confederate acting as a zoo visitor retrieved a reward from the box using a sequence of actions containing both causally relevant and irrelevant elements. Despite the absence of intentional demonstration, or social pressure to copy, a majority of both child and even adult observers included all causally irrelevant actions in their reproduction. This occurred even though causal irrelevance appeared manifest because of the transparency of the puzzle-box. That over-imitation occurred so readily in a naturalistic context, devoid of social interaction and pressure, suggests that humans are opportunistic social learners throughout the lifespan, copying the actions of other individuals even when these actions are not intentionally demonstrated, and their causal significance is not readily apparent. The disposition to copy comprehensively, even when a mere onlooker, likely provides humans, irrespective of their age, with a powerful mechanism to extract maximal information from the social environment.

Gilbert Dempster Fisher (1906–1985): the BBC's “Hut Man”, Scottish naturalist, children's author and radio broadcaster

As the BBC's “Hut Man”, Gilbert Dempster Fisher was a pioneer of radio broadcasting for children in Scotland in the 1940s and 1950s. Also a successful author of children's books on natural history, he based both his writings and his broadcasts on his observations of the wildlife that surrounded his isolated hut near Lochwinnoch, Renfrewshire. Devoted to pedagogy, he established “The Hut-Man's Club” for children in the late 1930s and was foremost in the encouragement of natural history in Scottish schools. He also wrote poetry for young children and, from 1947 to 1950, he produced The children's magazine. During the last decade of his “Hut life” he was engaged by Scottish local education authorities to speak in schools and residential camps about nature study, captivating children with his “Hut Man” tales. He also engaged with teachers to help them deliver natural history lessons, writing a comprehensive guide book on the subject. The teacher-training authorities, however, failed to capitalize on his vision of nature study within the school curriculum. Disillusioned by their intransigence and faced with local environmental degradation of the Hut Country and inappropriate housing development locally, he moved east. In 1956 he was appointed Director-Secretary of the Royal Zoological Society of Scotland administering Edinburgh Zoo. This paper concentrates on his “Hut Man” career as an author and radio presenter; the communication of natural history being its central theme, at a time when radio was becoming a popular medium of mass communication.

Prevalence of Entamoeba species in captive primates in zoological gardens in the UK.

The aim of this study was to determine the prevalence of amoebic infection in non-human primates (NHPs) from six Zoological gardens in the United Kingdom. Initially, 126 faecal samples were collected from 37 individually identified NHPs at Twycross Zoo, UK, and were subjected to microscopic examination. A subsequent, nationwide experiment included 350 faecal samples from 89 individually identified NHPs and 73 unidentified NHPs from a number of UK captive wildlife facilities: Twycross Zoo (n = 60), Colchester Zoo (n = 3), Edinburgh Zoo (n = 6), Port Lympne Wild Animal Park (n = 58), Howletts Wild Animal Park (n = 31), and Cotswold Wildlife Park (n = 4). Samples were examined by PCR and sequencing using four specific primer sets designed to differentiate between the pathogenic E. histolytica, the non-pathogenic E. dispar, and non-pathogenic uninucleate cyst-producing Entamoeba species. In the first experiment, Entamoeba was detected in 30 primates (81.1%). Six (16.2%) primates were infected with E. histolytica species complex. The highest carriage of Entamoeba species was found in Old World Colobinae primates. In the nationwide experiment, molecular analysis of faecal samples revealed notable rates of Entamoeba infection (101 samples, 28.9%), including one sample infected with E. histolytica, 14 samples with E. dispar, and 86 samples with uninucleated-cyst producing Entamoeba species. Sequences of positive uninucleated-cyst producing Entamoeba samples from Twycross Zoo clustered with the E. polecki reference sequences ST4 reported in Homo sapiens, and are widely separated from other Entamoeba species. These findings suggest a low prevalence of the pathogenic Entamoeba infection, but notable prevalence of non-pathogenic E. polecki infection in NHPs in the UK.

Conservation at work

Abstract Simon Girling, Head of Veterinary Services at Edinburgh Zoo, has been instrumental in the efforts to breed giant pandas in Scotland.

Interspecific interactions and welfare implications in mixed species communities of capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) over 3 years

Species have complex relationships with others in the wild, and some such as capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) naturally choose to associate with each other. There are a number of benefits of exhibiting such species in correspondingly mixed communities in captivity to enhance welfare through increased social complexity, which is potentially environmentally enriching in restricted captive enclosures. Monitoring the interactions between species is critical, however, particularly when members of one species are considerably larger and potentially more aggressive than the other. We report on the frequency and nature of interspecific interactions between S. apella and S. sciureus during four time periods over 3 years (2008–2010) following the formation of two mixed species groups at the ‘Living Links to Human Evolution’ Research Centre in Edinburgh Zoo, Scotland. Both the rate and the distribution of interspecific interactions among aggressive, affiliative and neutral categories of behaviour varied over time (P<0.05). We predicted that S. apella would engage in more interspecific, particularly aggressive, interactions than S. sciureus than vice versa, as they are the larger, more social species and have a more pugnacious temperament. This was the case overall (P<0.05), and particularly in 2009 and 2010. We predicted that affiliative interactions would increase over time as the number of youngsters increased and as the youngsters grew up together, establishing equable relationships and “territorial” boundaries. The data did not support this prediction. Both the most affiliative and least aggressive interspecific interactions were observed following internal enclosure refurbishment in 2008 and hence we argue that good enclosure design and husbandry is the most important factor in promoting positive interactions between individuals in mixed species groups. We conclude that long-term monitoring is important, and when combined with appropriate husbandry and enclosure upkeep, the welfare of individuals is enhanced in mixed species groups by the presence of other species.

Husbandry training, using positive reinforcement techniques, for Marabou stork Leptoptilos crumeniferus at Edinburgh Zoo

Positive reinforcement training utilizes operant conditioning through intentionally pairing a reward with a desired behaviour. Despite frequent use in the husbandry of mammals in captivity, these techniques are rarely incorporated in avian husbandry protocols. Marabou stork Leptoptilos crumeniferus managers are encouraged to use husbandry training to combat frequently encountered management problems. Marabous can be aggressive in captivity, requiring careful management during introductions, flexibility when choosing individuals to house together and a sound understanding of Marabou stork behaviour. Susceptibility to foot problems means that Marabou storks need indoor housing during cold weather and their feet should be monitored. At the Royal Zoological Society of Scotland Edinburgh Zoo, a training programme was incorporated into the daily care of a pair of Marabou storks. This programme included clicker training and stationing, pair introduction, house training, health checks (including scale training) and crate training. Here, training experiences relating to this programme are presented, with additional reference to a similar programme run at Disney's Animal Kingdom, FL, USA. Through training, we were able to ease the process of moving birds, reduce aggression and regularly monitor health in a low‐stress manner. We demonstrate that husbandry training can be effective without excessive time or staff costs, and can be rewarding for both birds and trainers.

Network Analysis of Social Changes in a Captive Chimpanzee Community Following the Successful Integration of Two Adult Groups

Chimpanzees are highly territorial and have the potential to be extremely aggressive toward unfamiliar individuals. In the wild, transfer between groups is almost exclusively completed by nulliparous females, yet in captivity there is often a need to introduce and integrate a range of individuals, including adult males. We describe the process of successfully integrating two groups of chimpanzees, each containing 11 individuals, in the Budongo Trail facility at the Royal Zoological Society of Scotland's Edinburgh Zoo. We use social network analysis to document changes in group dynamics within this population over the 16 months following integration. Aggression rates were low overall and members of the two original groups engaged in significantly fewer aggressive interactions over time. Association and grooming data indicate that relationships between members of the original groups became stronger and more affiliative with time. Despite these positive indicators the association data revealed the continued existence of two distinct subgroups, a year after integration. Our data show that when given complex space and freedom to exhibit natural fission-fusion groupings, in which the chimpanzees choose whom they wish to associate and interact with, the building of strong affiliative relationships with unfamiliar individuals is a very gradual process.

Zoo visitors' understanding of terms denoting research activity.

Zoos have increasingly sought to justify their existence by reference to a scientific role particularly in the domains of animal welfare and conservation. Given recent initiatives by the UK government to foster public engagement with science, it is timely to investigate public attitudes towards primary research activity by zoos. This study reports the views of 83 visitors to Edinburgh Zoo. Within certain items in a structured interview noun terms denoting research activity were manipulated ("research" versus "studies") as was their qualification (adjective "scientific" present or absent before the noun term). "Research" was associated with a restricted and negative perception of investigatory activity. This effect was intensified when the noun term was preceded by "scientific". It is concluded that there is a continuing need to challenge public perceptions, particularly of the phrase "scientific research"; that in the meantime zoos should perhaps exercise caution when using it in relation to their activities.

Assessing Public Engagement with Science in a University Primate Research Centre in a National Zoo

Recent years have seen increasing encouragement by research institutions and funding bodies for scientists to actively engage with the public, who ultimately finance their work. Animal behaviour as a discipline possesses several features, including its inherent accessibility and appeal to the public, that may help it occupy a particularly successful niche within these developments. It has also established a repertoire of quantitative behavioural methodologies that can be used to document the public's responses to engagement initiatives. This kind of assessment is becoming increasingly important considering the enormous effort now being put into public engagement projects, whose effects are more often assumed than demonstrated. Here we report our first attempts to quantify relevant aspects of the behaviour of a sample of the hundreds of thousands of visitors who pass through the ‘Living Links to Human Evolution Research Centre’ in Edinburgh Zoo. This University research centre actively encourages the public to view ongoing primate research and associated science engagement activities. Focal follows of visitors and scan sampling showed substantial ‘dwell times’ in the Centre by common zoo standards and the addition of new engagement elements in a second year was accompanied by significantly increased overall dwell times, tripling for the most committed two thirds of visitors. Larger groups of visitors were found to spend more time in the Centre than smaller ones. Viewing live, active science was the most effective activity, shown to be enhanced by novel presentations of carefully constructed explanatory materials. The findings emphasise the importance and potential of zoos as public engagement centres for the biological sciences.

The ‘Living Links to Human Evolution’ Research Centre in Edinburgh Zoo: a new endeavour in collaboration

The ‘Living Links to Human Evolution’ Research Centre in Edinburgh Zoo has been designed as a scientific institution managed in a collaboration between the Royal Zoological Society of Scotland, the University of St Andrews and the Scottish Primate Research Group, which represents a consortium of primatologists at the Universities of St Andrews, Stirling, Abertay, Aberdeen and Edinburgh. The Centre has been created to facilitate behavioural, cognitive and welfare-based research on naturalistically housed monkeys, at the same time introducing the zoo-visiting public to the science embodied in these enterprises, in an educational and even entertaining way. This article outlines the development of this collaboration, the details of how the Centre operates and reports on its early successes.

Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management

Social network analysis (SNA) is rapidly gaining popularity in primatology, but its application to the management of zoo-housed primates has been largely overlooked. Here I use SNA techniques to explore the social structure of chimpanzees (Pan troglodytes) housed in the new "Budongo Trail" exhibit at Edinburgh Zoo, UK. Given that individuals have extensive space (2332 m(2)), and access to several interconnected exhibit sections, I test the hypothesis that individuals are able to choose to interact with specific social partners. Spatial association and social interaction data were recorded from 400 focal watches on 11 individuals, and association, affiliative, and agonistic networks were constructed. Matrix correlations showed that individuals who spent time in close proximity were likely to affiliate with one another, but spatial association did not predict the frequency of agonistic encounters. Cluster analysis revealed significantly distinct sub-groups in the affiliative network (but not association or agonistic networks) in line with maternal kinship. Overall my findings support the hypothesis that the Budongo Trail exhibit facilitates the expression of social preferences, and suggests that SNA can be a useful tool to study zoo primates when proximity between individuals is not forced (i.e. in large, modern exhibits). Now that I have validated a set of SNA methods for this community, they can be used to trace changes in social dynamics over a longer time period, and ultimately assist zoo staff in their management decisions.

Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus)

There are potential advantages of housing primates in mixed species exhibits for both the visiting public and the primates themselves. If the primates naturally associate in the wild, it may be more educational and enjoyable for the public to view. Increases in social complexity and stimulation may be enriching for the primates. However, mixed species exhibits might also create welfare problems such as stress from interspecific aggression. We present data on the behavior of single and mixed species groups of capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) housed at the Living Links to Human Evolution Research Centre in the Royal Zoological Society of Scotland's Edinburgh Zoo. These species associate in the wild, gaining foraging benefits and decreased predation. But Cebus are also predators themselves with potential risks for the smaller Saimiri. To study their living together we took scan samples at > or =15 min intervals on single (n=109) and mixed species groups (n=152), and all occurrences of intraspecific aggression and interspecific interactions were recorded. We found no evidence of chronic stress and Saimiri actively chose to associate with Cebus. On 79% of scans, the two species simultaneously occupied the same part of their enclosure. No vertical displacement was observed. Interspecific interactions were common (>2.5/hr), and equally divided among mildly aggressive, neutral, and affiliative interactions such as play. Only one aggressive interaction involved physical contact and was non-injurious. Aggressive interactions were mostly (65%) displacements and vocal exchanges, initiated almost equally by Cebus and Saimiri. Modifications to the enclosure were successful in reducing these mildly aggressive interactions with affiliative interactions increasing in frequency and diversity. Our data suggest that in carefully designed, large enclosures, naturally associating monkeys are able to live harmoniously and are enriched by each other.

Within-group differences in captive Diana monkey (Cercopithecus diana diana) behaviour

This case study examines the activity budgets of captive Diana monkeys (Cercopithecus diana diana) and discusses results in the context of what is known regarding captive and wild-type behaviour in this species and other guenons. The activities of a family group of Diana monkeys (two parents and four offspring) housed at Edinburgh Zoo, UK, were quantified using a 5-min interval scan sampling technique. The 5100 observation points collected showed that the subjects spent the largest proportion of their time observing (approx. 46%), followed by feeding (approx. 15%), playing (approx. 11%), mutual grooming (approx. 8%) and resting (approx. 7%). The daily activity budgets for each of the subjects were tallied and, at the end of the 10-day observation period, used to produce a data matrix consisting of nine behaviour variables per subject. Clear among-individual differences in activity were identified with canonical discriminant function analysis. This multivariate approach illustrated how the combined behaviours of the parent male were distinct from those of the rest of the family group. Within the remainder of the group, the three youngest offspring displayed similar activity budgets, whereas the overall behaviour of the eldest offspring (a female) was between that of its siblings and her mother.