Current status and future directions of applied behavioral research for animal welfare and conservation

The papers that follow in this special issue reflect the state of knowledge and theory in the fields of animal welfare and conservation behavior. A particular focus is placed on how enrichment can be used judiciously to improve welfare and to prepare captive animals for release back to the wild. However, my purpose here is not simply to reiterate what the contributors of this special issue have said, but to provide an overview of the major themes, problems, and opportunities in applied animal behavior related to conservation and welfare. I review major issues in three interrelated areas: captive welfare, captive breeding, and conservation behavior research for wild populations. Despite many advancements in welfare science, one of the most significant impediments to a predictive science of welfare is the need to further refine theories advanced to explain environment–welfare relationships. I provide a brief overview of ten theories that have been proposed to explain good or poor welfare and suggest that they need to be made more conceptually distinct so that clear hypotheses can be articulated, and predictions made and tested. Captive breeding programs for ex situ conservation have borrowed and applied many of the concepts involved in welfare science to great advantage. Other keys to successful breeding programs include applying knowledge of social organization and processes to enhance reproduction; for example, finding the right combination of individuals to get animals breeding. However, behaviorists are only recently learning how to manipulate behavioral mechanisms, such as signaling behavior and mate choice, to optimize captive breeding for conservation. The emerging field of conservation behavior has played a role in captive breeding, but also is poised to play a major role in in situ conservation. Applied behavioral research can illuminate a number of issues important to conservation, including behavioral responses to habitat fragmentation and human disturbance (e.g., pollutants, noise, and light), and human–animal conflict (e.g., crop-raiding). Behavioral decisions made when animals are dispersing and selecting habitat for settlement determine the distribution of animals on the landscape and are important to understand for improving reserve and habitat corridor design. Captive–release and translocation programs require detailed behavioral knowledge to predict responses to novel environments and ensure that animals are adequately prepared for environmental change. This review underscores that many of the behavioral processes of interest to welfare science are also important for conservation behavior: perception, stress, assessment and decision-making rules, and other behavioral and physiological mechanisms. If properly understood, these mechanisms can be manipulated in the service of conservation goals, moving the field of conservation behavior from implication to application. A better integration of the disciplines of animal welfare and conservation behavior – together tackling problems at multiple levels of analysis – will further these goals.     

What Is the Future for Zoos and Aquariums?

ABSTRACT

Animal welfare concerns have plagued the professional zoo and aquarium field for decades. Societal differences remain concerning the well-being of animals, but it appears a shift is emerging. Scientific studies of animal welfare have dramatically increased, establishing that many previous concerns were not misguided public empathy or anthropomorphism. As a result, both zoo and aquarium animal welfare policy and science are now at the center of attention within the world’s professional zoos and aquariums. It is now possible to view a future that embraces the well-being of individual captive exotic animals, as well as that of their species, and one in which professional zoos and aquariums are dedicated equally to advancing both. Though the ethics of keeping exotic animals and animals from the wild in captivity are still a contentious subject both outside and even within the profession, this study argues. We argue that this path forward will substantially improve most zoo and aquarium animals' welfare and could significantly reduce societal concerns. If animal welfare science and policy are strongly rooted in compassion and embedded in robust accreditation systems, the basic zoo/aquarium paradigm will move toward a more thoughtful approach to the interface between visitors and animals. It starts with a fundamental commitment to the welfare of individual animals.     

Effect of Enclosure Quality on Reactivity and Welfare of Captive Soemmerring's Gazelle (Gazella soemmerringii)

The welfare of nonhuman animals in zoos is a great challenge to the zookeeper. Changes in the behavioral response of captive animals to their immediate environment can be used as a method for evaluating their welfare status. This study evaluates reactive responses of 3 groups of captive Soemmerring's gazelle (Gazella soemmerringii) kept in enclosures of different quality at Giza Zoo, Egypt. The study ascribes variations in observed behaviors to the differences in the living standards of the 3 groups. The group most concealed from visitors' disturbance (Group 3) was the least reactive. With the morning onset of human-nonhuman animal interaction, reactivity reached significantly higher levels. The study noted no difference in reactivity between male and female animals. The main sign of the animals' alertness was their attention to sources of disturbances; vocalization was minimal. Animals in Groups 1 and 2, those most accessible to visitors, had higher agonistic reactions than animals in Group 3.     

非人灵长类饲养与管理过程中的福利保障

实验动物饲养管理和福利保障的问题已越来越被国际社会所关注.与发达国家相比,中国对实验动物福利的研究及大众化意识则相对滞后.中国作为世界上最大的实验灵长类动物的饲养与出口国,每年遭受的国际贸易损失始终位居全球首位.为此,本文引入了实验灵长类福利的"5个自由"理论:1)动物有避免干渴、饥饿和营养不良等不利因素影响的自由;2)动物有获得舒适生活条件的自由;3)动物有脱离痛苦、受伤和疾病骚扰的自由;4)动物有表达自然行为的自由;5)动物有脱离恐惧和心理压力的自由.在上述理论的基础上,提高实验动物福利应具体从饲养的物理环境、营养供给、饲养管理、繁殖管理及饲养环境的多样性等几方面着手.通过总结国际与此相关的研究进展,旨为中国相关研究提供素材和为完善国内现行的法规及标准提出一些思路.     

Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus)

Stereotyped behaviour occurs in a wide variety of captive animals including ursids. The provision of animal control over aspects of their environment by providing choices is a critical element for improving welfare. The behaviour of two sibling polar bears at a metropolitan zoo was examined to investigate the effect of providing access to their indoor, off-exhibit holding space. Both bears demonstrated behavioural changes when given the choice to access their indoor dens including decreased stereotyped behaviours and increased social play. These results, although based on just two bears, provide additional support for the assertion that choice and control are closely tied to issues of well-being for captive animals.     

Effect of Enclosure Quality on Reactivity and Welfare of Captive Soemmerring's Gazelle (Gazella soemmerringii)

The welfare of nonhuman animals in zoos is a great challenge to the zookeeper. Changes in the behavioral response of captive animals to their immediate environment can be used as a method for evaluating their welfare status. This study evaluates reactive responses of 3 groups of captive Soemmerring's gazelle (Gazella soemmerringii) kept in enclosures of different quality at Giza Zoo, Egypt. The study ascribes variations in observed behaviors to the differences in the living standards of the 3 groups. The group most concealed from visitors' disturbance (Group 3) was the least reactive. With the morning onset of human-nonhuman animal interaction, reactivity reached significantly higher levels. The study noted no difference in reactivity between male and female animals. The main sign of the animals' alertness was their attention to sources of disturbances; vocalization was minimal. Animals in Groups 1 and 2, those most accessible to visitors, had higher agonistic reactions than animals in Group 3.     

Philosophy of environmental enrichment: Past,present, and future

The brief tenure of environmental enrichment has been influenced both directly and indirectly by the field of psychology, from the work of B.F. Skinner to that of Hal Markowitz. Research on enrichment supports the supposition that an enriched environment does indeed contribute to a captive animal’s well‐being. Critical elements of effective environmental enrichment are 1) assessing the animal’s natural history, individual history, and exhibit constraints and 2) providing species‐appropriate opportunities, i.e., the animal should have some choices within its environment. This paper presents a historic perspective of environmental enrichment, proposes a broader, more holistic approach to the enrichment of animals in captive environments, and describes a framework or process that will ensure a consistent and self‐sustaining enrichment program. Zoo Biol 20:211–226, 2001. © 2001 Wiley‐Liss, Inc.     

Animal Welfare at the Group Level: More Than the Sum of Individual Welfare?

Currently assessment and management of animal welfare are based on the supposition that welfare status is something experienced identically by each individual animal when exposed to the same conditions. However, many authors argue that individual welfare cannot be seen as an ‘objective’ state, but is based on the animal’s own self-perception; such perception might vary significantly between individuals which appear to be exposed to exactly the same challenges. We argue that this has two implications: (1) actual perceived welfare status of individuals in a population may vary over a wide range even under identical environmental conditions; (2) animals that appear to an external observer to be in better or poorer welfare condition may all in fact perceive their own individual status as the same. This would imply that optimum welfare of a social group might be achieved in situations where individual group members differ markedly in apparent welfare status and perceive their own welfare as being optimal under differing circumstances. Welfare phenotypes may also vary along a continuum between self-regarding and other-regarding behaviour; a variety of situations exist where (social) individuals appear to invest in the welfare of other individuals instead of maximising their own welfare; in such a case it is necessary to re-evaluate individual welfare within the context of a social group and recognise that there may be consequences for the welfare of individuals, of decisions made at the group level or by other group members.     

Distressed Animal Behaviors and Some Recommendations for Improvements at the Kuala Lumpur Zoo,Malaysia

The artificial living conditions of captive animals present numerous challenges for animal caretakers. In this study I explored abnormal behaviors in certain caged animals at the Kuala Lumpur Zoo. Findings obtained from observations of animals and interviews of the zoo staff are followed by recommendations: including the development of standards and manuals, licensing of zoos and animals, and increased budgets from governments or alternative sources. Such interventions should bring considerable improvements in animal welfare at the zoos in the region.     

Distressed animal behaviors and some recommendations for improvements at the Kuala Lumpur Zoo, Malaysia

The artificial living conditions of captive animals present numerous challenges for animal caretakers. In this study I explored abnormal behaviors in certain caged animals at the Kuala Lumpur Zoo. Findings obtained from observations of animals and interviews of the zoo staff are followed by recommendations: including the development of standards and manuals, licensing of zoos and animals, and increased budgets from governments or alternative sources. Such interventions should bring considerable improvements in animal welfare at the zoos in the region.     

A Case Study of Malayan Tapir (Tapirus indicus) Husbandry Practice Across 10 Zoological Collections

The Malayan, or Asian, tapir (Tapirus indicus) has a diminishing wild population and is becoming more common in captivity as zoos attempt to manage sustainable ex situ populations. Tapirs can be relatively easy to maintain and breed, but captive animals appear to suffer from reduced activity budgets, obesity, and poor public image. A questionnaire‐based survey was designed and sent specifically to 10 collections around the world that exhibit Malayan tapirs, with the aim of assessing husbandry regimes to determine prevalence of standardized practices as well as highlighting any key differences, and to showcase good practice, thus providing information beneficial to those maintaining this species in their zoo. Twenty‐five animals were included in the survey from collections across four continents. The research's major conclusions show differing dietary make‐up, with a lack of forage provision, contrasting with a diverse array of enrichment protocols used. Significant differences were noted between zoos for total amount of food offered (P = 0.000) as well as ratios of forage to concentrate pellet offered (P = 0.004). Comparing food offered to male and female tapirs with published requirements for an “average” of either gender shows not all zoos providing the amount suggested in husbandry guidelines. Intelligently designed and original enrichment was provided to all animals but differences between zoos were noted in the application and “usefulness” of enrichment for individual tapir. Overall, animals are benefiting from enrichment but welfare could be further improved via consistent feeding of ad libitum forage and regular use of browse as a constituent part of daily rations. Zoo Biol. 32:347–356, 2013. © 2012 Wiley Periodicals, Inc.     

Exploring African lion (<Emphasis Type="Italic">Panthera leo</Emphasis>) behavioural phenotypes: individual differences and correlations between sociality,boldness and behaviour

Increasing our understanding of personality, at an individual and group level, is crucial to the pre-release assessment of social species within ex situ reintroduction programs. We conducted the first exploration into the personality of a captive-origin pride of African lions (Panthera leo), assessing behavioural variations and consistencies in daily activity, social and hunting behaviour, and boldness. Data were collected via direct observations, while a species-specific protocol for testing boldness, using playbacks, was developed. Differences in sex, age and session time for the activity budget were evaluated using Pearson correlations and repeated-measures ANOVA, while social interactions were analysed using social network analysis. Spearman’s correlations were conducted to assess for associations between boldness scores, activity and sociality. The two boldness tests provided a range of scores per lion, indicating that the test was effective. Correlations and variations in individual behaviour indicated that adults and sub-adults have specific roles within pride behaviour. Correlations between boldness and activity and social behaviours provided information on the role of individuals, allowing investigation into the behaviour of a dominant and a social keystone. Our study indicates that evaluating various aspects of behaviour in conjunction with boldness has the potential to assist the pre-release assessment of a pride within an ex situ reintroduction program.     

Innovation in chimpanzees

The study of innovation in non‐human animals (henceforth: animals) has recently gained momentum across fields including primatology, animal behaviour and cultural evolution. Examining the rate of innovations, and the cognitive mechanisms driving these innovations across species, can provide insights into the evolution of human culture. Especially relevant to the study of human culture is one of our closest living relatives, the chimpanzee (Pan troglodytes). Both wild and captive chimpanzees demonstrate an impressive ability to innovate solutions to novel problems, but also a striking level of conservatism in some contexts, creating a unique and at times puzzling, picture of animal innovation. Whilst the animal innovation field is rife with potential for expanding our knowledge of human and non‐human cognition and problem‐solving, it is undermined by a lack of consistency across studies. The field is yet to settle on a definition of the term ‘innovation’, leading to studies being incomparable across and even within the same species. Here, we fill two gaps in the literature. First, we discuss some of the most prevalent definitions of ‘innovation’ from different fields, highlighting similarities and differences between them. Secondly, we provide an up‐to‐date review of accounts of innovations in both wild and captive chimpanzees. We hope this review will provide a resource for researchers interested in the study of innovation in chimpanzees and other animals, as well as emphasising the need for consistency in the way in which innovations are reported.     

Visitors' Effects on the Welfare of Animals in the Zoo: A Review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

Visitors' effects on the welfare of animals in the zoo: a review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

The effects of enriching laboratory cages using various physical structures on multiple measures of welfare in singly-housed rats

The single housing of laboratory rats may be recommended in some situations such as hypothesis-driven or test-specific studies, during electroencephalogram recording of phases of sleep and after surgical procedures. However, as single housing of laboratory rats has been shown to be stressful, modification of the housing environment is needed to improve the welfare of these animals. This experiment was carried out to investigate the long-term effects of environmental enrichment on some behavioural, physiological, pathological and psychological measures of welfare. With two batches of animals, 24 rats were housed singly in either enriched cages (EC) (n = 12 cages) or unenriched cages (UC) (n = 12 cages). Behaviour was sampled every week and so was body weight and weight gain over a six-week observation period. Behaviours of the rats in the elevated plus-maze were recorded on the seventh week, whereas organ weights were recorded postmortem. The results revealed that long-term single housing of rats in super-enriched cages increased levels of indicators of good welfare including sleep, exploration, movement and feeding behaviour, body weights, weight gains and the relative weights of the thymus gland and spleen, and decreased levels of indicators of poor welfare such as stationary behaviour and the relative weight of adrenal glands. Thus, enrichment of conventional cages of newly weaned singly-housed laboratory rats with multiple physical structures appeared to improve their ability to control the environment and to promote their species-specific behaviour; changes that can ultimately result in good welfare.     

Review: From human–animal relation practice research to the development of the livestock farmer's activity: an ergonomics–applied ethology interaction

Animal husbandry and working conditions for livestock farmers have changed significantly in recent years as agriculture has been exposed to economic as well as health, environmental and ethical challenges. The idea of interdependent welfare between humans and animals is more relevant now than ever. Here, we innovatively bridge two disciplines—ergonomics and applied ethology—to achieve an in-depth observational understanding of real husbandry practice (by farmers, inseminators, vets) at work. Ergonomics aims to gain a detailed understanding of human activity in its physical, sensitive and cognitive dimensions in relation to a task. It also aims to transform work situations through a systemic approach drawing on multiple levers for change. Here, we examine how this analysis holds up to the inclusion of animals as an integral component of the livestock farmer’s work situation. Applied ethology studies behaviours in animals managed by humans. It aims to understand how these animals perceive their environment, including how they construct their relationship with the livestock farmer. This paper proposes an original conception of the human–animal relationship in animal husbandry that employs core structural concepts from both disciplines. From an ergonomic point of view, we address the human–animal relations by examining the relationship between ‘prescribed’ and real work practices, between work and personal life situation, between professional task and human activity. On the applied ethology side of the equation, the human–animal relationship is a process built through communication and regular interactions between two ‘partners’ who know each other. The goal is to understand how each partner perceives the other according to their multimodal sensory world and their cognitive and emotional capacities, and to predict the outcome of future interactions. We cross-analyse these scientific views to show, based on examples, how and in what way they can intersect to bring better analysis of these human–animal relationships. We reflect on common working hypotheses and situated observational approaches based on indicators (behaviour and animal and human welfare/health). This analysis prompts us to clarify what human–animal relational practice means in animal husbandry work, i.e. a strategy employed by the livestock farmer to work safely and efficiently in a healthy environment, where the animal is treated as a partner in the relationship. In this perspective, the challenge is for the livestock farmer’s activity to co-build a positive relationship and avoid being subject to this one.     

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.)

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.     

Health and Welfare in Animals and Humans

This paper contains a brief comparative analysis of some philosophical and scientific discourses on human and animal health and welfare, focusing mainly on the welfare of sentient animals. The paper sets forth two kinds of proposals for the analysis of animal welfare which do not appear in the contemporary philosophical discussion of human welfare, viz. the coping theory of welfare and the theory of welfare in terms of natural behaviour. These proposals are scrutinized in the light of some similar theories dealing with human health and quality of life. My conclusion is that the coping theory and the natural behaviour theory are not in themselves adequate for the characterization of welfare, either for humans or for sentient animals. I contend, finally, that, in the light of the previous discussion, there are good arguments for a particular set of analyses of both animal and human welfare, viz. the ones that are based on the notions of preference satisfaction and positive subjective experiences.     

In pursuit of peak animal welfare; the need to prioritize the meaningful over the measurable

Despite the diversity of animal welfare definitions, most recognise the centrality of the feelings of animals which are currently impossible to measure directly. As a result, animal welfare assessment is heavily reliant upon the indirect measurement of factors that either affect what animals feel, or are effected by how they feel. Physiological and health orientated measures have emerged as popular metrics for assessing welfare because they are quantifiable, can effect and be affected by how animals feel and have merits regardless of their relationship to the feelings of animals. However, their popularity in animal welfare assessment has led to them having a disproportionate influence on animal management to the detriment of animal welfare in numerous instances. Here, the case is made that a tension exists between management that prioritizes aspects of care reflecting popular animal welfare metrics such as those relating to physical health, and management that emphasizes psychological wellbeing. By re‐examining the relative merits of physical and psychological priorities in animal management, an alternate animal welfare paradigm emerges less tied to traditional welfare metrics. This paradigm theorizes about the possibility for an optimal animal welfare state to exist where managed animal populations provided essential psychological outlets but protected from key physical stressors routinely experienced in the wild, might experience higher levels of welfare than wild populations would routinely experience. The proposition that optimal animal welfare could theoretically be achieved in well managed and well designed captive environments challenges a widely held ethical perspective that captivity is inherently bad for animal welfare.