Human-animal interactions and machine-animal interactions in animals under human care: A summary of stakeholder and researcher perceptions and future directions.

Animals under human care are exposed to a potentially large range of both familiar and unfamiliar humans. Human-animal interactions vary across settings, and individuals, with the nature of the interaction being affected by a suite of different intrinsic and extrinsic factors. These interactions can be described as positive, negative or neutral. Across some industries, there has been a move towards the development of technologies to support or replace human interactions with animals. Whilst this has many benefits, there can also be challenges associated with increased technology use. A day-long Animal Welfare Research Network workshop was hosted at Harper Adams University, UK, with the aim of bringing together stakeholders and researchers (n = 38) from the companion, farm and zoo animal fields, to discuss benefits, challenges and limitations of human-animal interactions and machine-animal interactions for animals under human care and create a list of future research priorities. The workshop consisted of four talks from experts within these areas, followed by break-out room discussions. This work is the outcome of that workshop. The key recommendations are that approaches to advancing the scientific discipline of machine-animal interactions in animals under human care should focus on: (1) interdisciplinary collaboration; (2) development of validated methods; (3) incorporation of an animal-centred perspective; (4) a focus on promotion of positive animal welfare states (not just avoidance of negative states); and (5) an exploration of ways that machines can support a reduction in the exposure of animals to negative human-animal interactions to reduce negative, and increase positive, experiences for animals.

The Impact of Visitors on Non-Primate Species in Zoos: A Quantitative Review.

Visitors are a prominent feature in the lives of zoo animals, and their presence can cause a range of impacts on zoo animals (typically classed as positive, negative or neutral impacts), commonly referred to as the 'visitor effect'. This paper quantitatively collates the literature on the visitor effect in non-primate species, investigates the types of measures used to assess impacts of visitors on animals and considers whether impacts vary across non-primate species in zoos. In total, there were 105 papers which had investigated the impact of zoo visitors on 252 non-primate species/species groups. There has been a steady increase in visitor effect research in zoos since 2012 and this body of work incorporates species from avian (28% study species), reptilian (9%), amphibian (2%), fish (4%) and invertebrate taxa (1%). However, there is still a bias towards mammalian species (56%). The response to visitors varied across taxa. Amphibians responded negatively to visitors more frequently than would be expected by chance (p < 0.05), birds responded neutrally more frequently than would be expected by chance (p < 0.05) and fish responded neutrally and 'unknown' more frequently than would be expected by chance (p < 0.05). This review highlighted a number of animal-based metrics which have been used to assess the impacts of visitors on animals, with measures used varying across taxa. Moving forwards, it is recommended that moving forwards researchers incorporate a suite of measures, incorporating those which are meaningful in terms of being representative of individual animal experiences and animal welfare, collected in a manner which should capture those metrics accurately.

The Impact of COVID-19 Zoo Closures on Behavioural and Physiological Parameters of Welfare in Primates.

Primates are some of the most cognitively advanced species held in zoos, and their interactions with visitors are complex. The COVID-19 pandemic provided a unique opportunity to understand the impact of zoo visitors on animals, in comparison to "empty zoos". This study sought to understand the impact of facility closures and subsequent reopenings on behavioural and physiological parameters of welfare in four primate species housed in the UK: bonobos (Pan paniscus) (n = 8), chimpanzees (Pan troglodytes) (n = 11), and western lowland gorillas (Gorilla gorilla gorilla) (n = 6) held at Twycross Zoo (TZ); and olive baboons (Papio anubis) (n = 192) held at Knowsley Safari (KS). Behavioural data were collected from April-September 2020 (KS) and November 2020-January 2021 (TZ). Faecal samples were collected during morning checks from October-November (TZ) and July-November 2020 (KS). Faecal glucocorticoid metabolites (FGMs) were measured using ELISA kits. Statistical analysis for behavioural observations was undertaken using general linear models. Enclosure usage was assessed using t-tests and Mann-Whitney U-tests as appropriate. Bonobos and gorillas spent less time alone when facilities were open to the public (p = 0.004, p = 0.02 respectively). Gorillas spent less time resting when the facility was open to the public (p = 0.04), and chimpanzees engaged in more feeding (p = 0.02) and engagement with enrichment (p = 0.03) when the zoo was open to the public than when it was closed. Olive baboons performed less sexual and dominance behaviour and approached visitor cars more frequently when the safari park was opened to the public than they did the ranger's vehicle during closure periods. There were no significant changes in physiological parameters for any of the study species. The results suggest variable impacts of the zoo closures on zoo-housed primates. We recommend future work that seeks to understand the impact of individual-level differences on "visitor effects" and that differences between animal experiences in zoos and safari parks are further explored in a range of species.

Why Are Enrichment Practices in Zoos Difficult to Implement Effectively?

The good intentions of zoos to introduce enrichment practices that stimulate animals mentally and physically are not always achievable. Changes to the policies and procedures in organisations are difficult to fulfil for a range of reasons frequently investigated in change management literature. The implementation of these changes can be the source of ineffective attempts to generate positive interventions in organisations. In this study, we investigate whether interventions to improve animal management in zoos through enrichment are subject to implementation impediments. Qualitative data gathered from interviews with 23 keepers working with big cats across 12 zoos globally provided valuable insights into the barriers and enablers to the implementation of enrichment. Keepers participated voluntarily and worked in accredited zoos across Australia, New Zealand, Europe, south-east Asia, South Africa, and the United States of America. Thematic analysis of the data revealed five key themes that described some of the challenges zoos and keepers experience when implementing enrichment for big cats, in their words: "let's just be cautious", "purely surviving", "struggle to understand the goal", "can't always provide what you should", and "judge the effectiveness". These themes provide additional insights into potential areas for improvement, including greater attention to the benefits of enrichment for animal mental health and increased transparency around enrichment objectives in zoos.

Furred and feathered friends: How attached are zookeepers to the animals in their care?

Keeper-animal relationships (KARs) appear to be important in zoos, since they can enhance the well-being of both the animals and the keepers, can make animal husbandry easier, but conversely might risk inappropriate habituation of animals and possible risks to the safety of keepers. It is, therefore, important to know more about the variables involved in relationship formation. Here we use a modified version of the Lexington Attachment to Pets Scale (LAPS) to measure the strength of KARs between keepers and animals in their care, both in the zoo and in the home. LAPS questionnaires were completed by 187 keepers in 19 different collections across three countries. LAPS scores for attachment to zoo animals (ZA) were significantly lower than for pet animals (PA). There was no significant difference in ZA scores between different taxa, but there were significant taxon differences between PA scores. There were significant differences in both ZA and PA scores between different collections. Female respondents scored more highly than males for both ZA and PA. Multiple regression revealed that location, gender, and time spent with animals were significant predictors for ZA, while only gender and taxon were significant predictors for PA. It was concluded that PA scores were comparable with those for the general public, and reflected strong attachment of keepers to their pets, while ZA scores, although also reflecting attachment, were influenced by differences in institutional culture.

Bonded by nature: Humans form equally strong and reciprocated bonds with similar raised dogs and wolves.

Introduction: To explore human-canid relationships, we tested similarly socialized and raised dogs (Canis familiaris) and wolves (Canis lupus) and their trainers in a wildlife park. The aims of our study were twofold: first, we aimed to test which factors influenced the relationships that the trainers formed with the dogs or wolves and second, we investigated if the animals reacted to the trainers in accordance with the trainers' perceptions of their relationship. Methods: To achieve these goals, we assessed the relationships using a human-animal bonds survey, which the trainers used to rate the bonds between themselves and their peers with the canids, and by observing dyadic trainer-canid social interactions. Results: Our preliminary results given the small sample size and the set-up of the research center, demonstrate that our survey was a valid way to measure these bonds since trainers seem to perceive and agree on the strength of their bonds with the animals and that of their fellow trainers. Moreover, the strength of the bond as perceived by the trainers was mainly predicted by whether or not the trainer was a hand-raiser of the specific animal, but not by whether or not the animal was a wolf or a dog. In the interaction test, we found that male animals and animals the trainers felt more bonded to, spent more time in proximity of and in contact with the trainers; there was no difference based on species. Discussion: These results support the hypothesis that wolves, similarly to dogs, can form close relationships with familiar humans when highly socialized (Canine Cooperation Hypothesis). Moreover, as in other studies, dogs showed more submissive behaviors than wolves and did so more with experienced than less experienced trainers. Our study suggests that humans and canines form differentiated bonds with each other that, if close, are independent of whether the animal is a wolf or dog.

Indoors or Outdoors? An International Exploration of Owner Demographics and Decision Making Associated with Lifestyle of Pet Cats.

Outdoor access for owned domestic cats (Felis catus) is a divisive issue. Cat safety, mental and physical wellbeing, infectious diseases, and wildlife depredation are cited as factors influencing owners; however, the degree of consideration each factor receives has not been quantified. This study (i) analysed which demographic variables are associated with greater odds of cats having indoor or outdoor lifestyles, (ii) identified which factors owners consider when making a choice on lifestyle and any regional variations, and (iii) identified if owners consider the different lifestyle options available and recognise their associated benefits. A series of online surveys were used for data collection. Binary logistic regression models were used to generate odds ratios assessing if demographic variables were significantly associated with cat lifestyle. Quantitative analysis of factors considered when deciding on cat lifestyle was accompanied by a thematic analysis of rich-text open-ended responses, providing nuanced insight into the rationale and elucidating additional factors considered. Of the demographic variables tested, 10/12 were significantly associated with lifestyle. Variables with higher odds of indoor-only lifestyles were owners being 26-35 years old, multi-cat households, junior cats, pedigree cats or unknown pedigree status, cats with health issues, living in city centres or urban areas, or living in the United States, Canada, Australia, or New Zealand. Variables with higher odds of indoor-outdoor lifestyles were owners being 46-55 years old or 56+ years old, households with residents 17 years old or under, male cats, and cats being mature or senior. Road traffic concerns were the most cited reason for keeping indoor-only cats across all global regions. The second-most cited reason varied regionally. For Europe, it was protection from people. For the USA and Canada, the reason was protection from wildlife, and for Australia and New Zealand, to prevent hunting. Indoor-outdoor cat owners cited most frequently the benefits to their cat's mental health. Over two-thirds of owners did not consider the alternative lifestyle for their cat. These data give insight into the priorities of cat owners with regards to feline wellbeing, feline safety, and wildlife depredation, helpful for individuals or organisations working with human behaviour change. They provide evidence that the numbers of indoor-only cats are likely to rise with increasing urbanisation. Finally, the data identify cat populations who may be at risk of compromised welfare due to unsuitable, or under-researched, lifestyles.

Understanding impacts of zoo visitors: Quantifying behavioural changes of two popular zoo species during COVID-19 closures.

Visitors are normally a prominent and constant feature in a zoo animals' environment with more than 700 million people visiting zoos and aquariums worldwide, annually. Animal-visitor interactions can be enriching and stimulating and are now considered within the Five Domains of animal welfare assessment. Zoo closures as a result of COVID-19 provided a unique opportunity to monitor the impact of abrupt and prolonged removal of visitors on two popular zoo species. Data were collected at four facilities (n = 3 slender-tailed meerkats, n = 1 African penguin) during COVID-19 zoo closures and up to one month following reopening to the public. Meerkats showed increased positive social interactions, increased alert behaviours, and reduced environmental interactions in the first month post-opening, as compared to closure periods. They also used more of their enclosures during periods of closure and spent longer than would be expected in zones furthest from visitor viewing areas when facilities reopened. African penguins showed no behavioural change between open and closure periods. Enclosure usage during both observation periods was relatively even and no differences were observed in enclosure use between open and closure periods. These results will enable an advanced understanding of the impact that people have on the behaviour of zoo animals, which has ramifications for animals used in close encounters and other 'visitor experiences' in the future. Understanding relationships between animals and people is applicable in all managed animal settings. The results from this study are of practical use in managing visitor access to animals moving forwards, including enclosure location and design, to ensure a positive visitor experience that does not negatively impact animal behaviour.

Zoo-housed mammals do not avoid giving birth on weekends.

There is evidence that zoo visitor presence can influence the behaviour and, in some cases, adrenal response of zoo animals, and can sometimes compromise animal welfare. In some laboratory studies, significantly more primate births have been reported on weekends, when fewer people are working there, compared with weekdays when staffing levels are at their highest. Here, we investigate whether there is evidence of a "weekend effect" on births in zoo animals as a result of visitor numbers. Unlike laboratories, zoos are typically busier with visitors on weekends than on weekdays, although staffing levels remain fairly consistent across days of the week. If zoo animal parturition is sensitive to human presence, then fewer births would be expected on weekends compared with weekdays. We tested this using birth data and visitor numbers on the entrance gate from zoo records across 16 species representing artiodactyls, perissodactyls, carnivores and primates at four British zoos, to see whether there is an association between mean daily birth rates and average visitor numbers. We predict that, if there is a visitor effect, daily births should be lower on weekends than weekdays and should correlate with mean daily visitor numbers. Results showed that births for all 16 species were randomly distributed through the week, and there was no significant decline in births on weekends. We conclude that the "weekend effect", if such a thing exists, does not appear to be a feature of zoo births, suggesting that elevated weekend visitor numbers are not sufficiently stressful to trigger delayed parturition.

Using Zoo Welfare Assessments to Identify Common Issues in Developing Country Zoos.

Zoo animal welfare is a high priority for many institutions worldwide, with modern zoos now ensuring that animals are housed and cared for to the highest standards. However, in countries where this knowledge is not as available or understood, standards may be lower. The aim of this research was to investigate if there were common zoo welfare concerns across developing country zoos. Wild Welfare is a charity working globally to improve welfare for zoo animals and has an independent welfare audit that is carried out before any intervention occurs. The Wild Welfare Audit, consisting of 110 questions, covering nine topics, was completed at 11 zoos in seven developing countries (Brazil, Egypt, Libya, Indonesia, Thailand, Malaysia and Vietnam) following a Likert scale score (1-3). A principal component analysis was also performed to evaluate the audit questions. The results suggest that common areas of concern were animal behaviour, positive animal mental states and human health and safety. These themes were likely due to the lack knowledge and understanding that may be linked to historical and cultural differences. This research has helped to revise the welfare audit as well as inform future intervention strategies for improving developing country zoo animal welfare.

A Retrospective Study of Macropod Progressive Periodontal Disease ("Lumpy Jaw") in Captive Macropods Across Australia and Europe: Using Data from the Past to Inform Future Macropod Management.

Macropod Progressive Periodontal Disease (MPPD) is a well-recognised disease that causes high morbidity and mortality in captive macropods worldwide. Epidemiological data on MMPD are limited, although multiple risk factors associated with a captive environment appear to contribute to the development of clinical disease. The identification of risk factors associated with MPPD would assist with the development of preventive management strategies, potentially reducing mortality. Veterinary and husbandry records from eight institutions across Australia and Europe were analysed in a retrospective cohort study (1995 to 2016), examining risk factors for the development of MPPD. A review of records for 2759 macropods found incidence rates (IR) and risk of infection differed between geographic regions and individual institutions. The risk of developing MPPD increased with age, particularly for macropods >10 years (Australia Incidence Rate Ratio (IRR) 7.63, p < 0.001; Europe IRR 7.38, p < 0.001). Prognosis was typically poor, with 62.5% mortality reported for Australian and European regions combined. Practical recommendations to reduce disease risk have been developed, which will assist zoos in providing optimal long-term health management for captive macropods and, subsequently, have a positive impact on both the welfare and conservation of macropods housed in zoos globally.

The Need for a Convergence of Agricultural/Laboratory and Zoo-based Approaches to Animal Welfare.

Advances in animal welfare science have led to a high number of studies published for farm, laboratory and zoo animals, with a huge breadth of innovative topic areas and methodologies. This paper investigates the different approaches used to undertake welfare research in farm, laboratory and zoo animals due to the variety of constraints that each group brings. We also set recommendations to how groups can support each other in moving forwards to reduce animal suffering and promote a life worth living, a goal that all parties aim to achieve. We propose that researchers develop more collaborations across species, in particular to focus on the applied component of animal welfare and utilizing positive welfare indicators; facilitate knowledge transfer and share good practice worldwide; and accept small n based studies that can still be scientifically robust and provide individual-based steps into advances in our knowledge. Ultimately, we need to be progressing animal welfare science to a point beyond legislative needs, and ensure that "high animal welfare" becomes an additional mission statement for all animal-based industries.

Using Qualitative Behaviour Assessment to Investigate Human-Animal Relationships in Zoo-Housed Giraffes (Giraffa camelopardalis).

Human-Animal Relationships (HAR) in zoos develop from repeated interactions between animals and their caretakers. HAR have been shown to affect health and welfare in farm animals, but limited zoo-based studies exist. This study investigates the association between the qualitative behaviour assessment (QBA) of emotional expression in giraffes and keeper action score in four types of keeper-animal interaction (KAI). Three giraffes generating 38 clips. QBA, using a free-choice profiling methodology, was applied instructing 18 observers to assess giraffe expressions shown in these clips. QBA scores were analysed using Generalized Procrustes Analysis. Keeper actions during each KAI event were rated by an independent marker, resulting in cumulative scores for keeper action quality. The association between QBA and the keeper action was analyzed using Spearman's rank correlations. Two main QBA dimensions were identified explaining 59% of the variation between clips. There were significant effects of giraffe and KAI type on QBA dimension 2 (inquisitive/impatient-calm/distracted), and significant positive associations between keeper action quality rating and QBA dimensions 1 and 2, indicating that positive keeper actions resulted in calm and confident giraffes with a willingness to interact. This is the first successful application of QBA for empirically addressing HARs in zoos, however given the small sample size of giraffes in this study, it can be regarded as a pilot study only, and further research is needed to validate the use of QBA in this context.

Advances in Applied Zoo Animal Welfare Science.

Nonhuman animal welfare science is the scientific study of the welfare state of animals that attempts to make inferences about how animals feel from their behavior, endocrine function, and/or signs of physical health. These welfare measurements are applicable within zoos yet inherently more complex than in farms and laboratories. This complexity is due to the vast number of species housed, lack of fundamental biological information, and relatively lower sample sizes and levels of experimental control. This article summarizes the invited presentations on the topic of "Advances in Applied Animal Welfare Science," given at the Fourth Global Animal Welfare Congress held jointly by the Detroit Zoological Society and the World Association of Zoos and Aquariums in 2017. The article focuses on current trends in research on zoo animal welfare under the following themes: (a) human-animal interactions and relationships, (b) anticipatory behavior, (c) cognitive enrichment, (d) behavioral biology, and (e) reproductive and population management. It highlights areas in which further advancements in zoo animal welfare science are needed and the challenges that may be faced in doing so.

Is wounding aggression in zoo-housed chimpanzees and ring-tailed lemurs related to zoo visitor numbers?

Chimpanzees in laboratory colonies experience more wounds on weekdays than on weekends, which has been attributed to the increased number of people present during the week; thus, the presence of more people was interpreted as stressful. If this were also true for primates in zoos, where high human presence is a regular feature, this would clearly be of concern. Here we examine wounding rates in two primate species (chimpanzees Pan troglodytes and ring-tailed lemurs Lemur catta) at three different zoos, to determine whether they correlate with mean number of visitors to the zoo. Wounding data were obtained from a zoo electronic record keeping system (ZIMS™). The pattern of wounds did not correlate with mean gate numbers for those days for either species in any group. We conclude that there is no evidence that high visitor numbers result in increased woundings in these two species when housed in zoos. Zoo Biol. 35:205-209, 2016. © 2016 Wiley Periodicals, Inc.

Keeper-Animal Interactions: Differences between the Behaviour of Zoo Animals Affect Stockmanship.

Stockmanship is a term used to describe the management of animals with a good stockperson someone who does this in a in a safe, effective, and low-stress manner for both the stock-keeper and animals involved. Although impacts of unfamiliar zoo visitors on animal behaviour have been extensively studied, the impact of stockmanship i.e familiar zoo keepers is a new area of research; which could reveal significant ramifications for zoo animal behaviour and welfare. It is likely that different relationships are formed dependant on the unique keeper-animal dyad (human-animal interaction, HAI). The aims of this study were to (1) investigate if unique keeper-animal dyads were formed in zoos, (2) determine whether keepers differed in their interactions towards animals regarding their attitude, animal knowledge and experience and (3) explore what factors affect keeper-animal dyads and ultimately influence animal behaviour and welfare. Eight black rhinoceros (Diceros bicornis), eleven Chapman's zebra (Equus burchellii), and twelve Sulawesi crested black macaques (Macaca nigra) were studied in 6 zoos across the UK and USA. Subtle cues and commands directed by keepers towards animals were identified. The animals latency to respond and the respective behavioural response (cue-response) was recorded per keeper-animal dyad (n = 93). A questionnaire was constructed following a five-point Likert Scale design to record keeper demographic information and assess the job satisfaction of keepers, their attitude towards the animals and their perceived relationship with them. There was a significant difference in the animals' latency to appropriately respond after cues and commands from different keepers, indicating unique keeper-animal dyads were formed. Stockmanship style was also different between keepers; two main components contributed equally towards this: "attitude towards the animals" and "knowledge and experience of the animals". In this novel study, data demonstrated unique dyads were formed between keepers and zoo animals, which influenced animal behaviour.

Cytogenetic analysis of paediatric astrocytoma using comparative genomic hybridisation and fluorescence in-situ hybridisation.

Little is known about the cytogenetic and molecular genetic events that lead to the formation of paediatric astrocytoma. We have analysed 57 paediatric astrocytoma (WHO grades I-IV) using comparative genomic hybridisation in order to identify common regions of abnormality. Large regions of copy number alterations were infrequent with 71% of tumours demonstrating no genomic imbalance. Furthermore, the most frequent aberrations (including gain of 6q, 2q, and 7q, and loss of 16 and 12q) occurred in only a subset of cases. High-copy number amplification was seen in five tumours at 12 different regions. The presence of copy number alterations was significantly associated with increasing grade of malignancy, and gain of 12q and the presence of high-copy number amplification were associated with a poor outcome in patients with malignant astrocytoma (P = 0.0039 and 0.0085, respectively). FISH analysis confirmed loss of 1p36 identified by CGH. There was no evidence of amplification of EGFR, CDK4, MET, CDK6, c-myc, or MDM2.