Thirty years after Brambell: whither animal welfare science?

It has been just over 30 years since the Brambell Committee issued its clarion call for research on the welfare of animals used in agriculture. What progress has farm animal welfare science made in those 30 years, and what challenges will it face in the next 30? In this article, I discuss the ways in which the Brambell report, with its emphasis on behavioral needs and suffering, both propelled and constrained the development of animal welfare science. The role that economic factors play and the ways in which they have imposed other kinds of constraints on scientists working with farm animals are also mentioned. Despite these constraints, animal welfare science has contributed to a number of significant improvements in the welfare of farm animals. There is, however, a growing sense that animal welfare science has reached an impasse and that ethical and scientific questions about animal welfare have become hopelessly entangled. In this context, I address what I view to be the principal challenge facing farm animal welfare science, namely to move the issue of beyond suffering to an evaluation of broader quality-of-life questions and their application to improvements in welfare.     

Toward a cross-species neuroscientific understanding of the affective mind: do animals have emotional feelings?

Do we need to consider mental processes in our analysis of brain functions in other animals? Obviously we do, if such BrainMind functions exist in the animals we wish to understand. If so, how do we proceed, while still retaining materialistic-mechanistic perspectives? This essay outlines the historical forces that led to emotional feelings in animals being marginalized in behavioristic scientific discussions of why animals behave the way they do, and why mental constructs are generally disregarded in modern neuroscientific analyses. The roots of this problem go back to Cartesian dualism and the attempt of 19th century physician-scientists to ground a new type of medical curriculum on a completely materialistic approach to body functions. Thereby all vitalistic principles were discarded from the lexicon of science, and subjective experience in animals was put in that category and discarded as an invalid approach to animal behavior. This led to forms of rigid operationalism during the era of behaviorism and subsequently ruthless reductionism in brain research, leaving little room for mentalistic concepts such as emotional feelings in animal research. However, modern studies of the brain clearly indicate that artificially induced arousals of emotional networks, as with localized electrical and chemical brain stimulation, can serve as "rewards" and "punishments" in various learning tasks. This strongly indicates that animal brains elaborate various experienced states, with those having affective contents being easiest to study rigorously. However, in approaching emotional feelings empirically we must pay special attention to the difficulties and vagaries of human language and evolutionary levels of control in the brain. We need distinct nomenclatures from primary (unconditioned phenomenal experiences) to tertiary (reflective) levels of mind. The scientific pursuit of affective brain processes in other mammals can now reveal general BrainMind principles that also apply to human feelings, as with neurochemical predictions from preclinical animal models to self-reports of corresponding human experiences. In short, brain research has now repeatedly verified the existence of affective experience-various reward and punishment functions-during artificial arousal of emotional networks in our fellow animals. The implications for new conceptual schema for understanding human/primate affective feelings and how such knowledge can impact scientific advances in biological psychiatry are also addressed.     

Behaviour as a tool in the assessment of animal welfare

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.     

A History of Animal Welfare Science

Human attitudes to animals have changed as non-humans have become more widely incorporated in the category of moral agents who deserve some respect. Parallels between the functioning of humans and non-humans have been made for thousands of years but the idea that the animals that we keep can suffer has spread recently. An improved understanding of motivation, cognition and the complexity of social behaviour in animals has led in the last 30 years to the rapid development of animal welfare science. Early attempts to define welfare referred to individuals being in harmony with nature but the first usable definition incorporated feelings and health as part of attempts to cope with the environment. Others considered that welfare is only about feelings but it is argued that as feelings are mechanisms that have evolved they are a part of welfare rather than all of it. Most reviews of welfare now start with listing the needs of the animal, including needs to show certain behaviours. This approach has used sophisticated studies of what is important to animals and has replaced the earlier general guidelines described as freedoms. Many measures of welfare are now used and indicate how good or how poor the welfare is. Naturalness is not a part of the definition of welfare but explains why some needs exist. In recent years, welfare has become established as one of various criteria used to decide on whether a system is sustainable because members of the public will not accept systems that cause poor welfare. The study of welfare has become part of the scientific basis upon which important political decisions are made.     

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.     

Aquatic animals, cognitive ethology, and ethics: questions about sentience and other troubling issues that lurk in turbid water

In this general, strongly pro-animal, and somewhat utopian and personal essay, I argue that we owe aquatic animals respect and moral consideration just as we owe respect and moral consideration to all other animal beings, regardless of the taxonomic group to which they belong. In many ways it is more difficult to convince some people of our ethical obligations to numerous aquatic animals because we do not identify or empathize with them as we do with animals with whom we are more familiar or to whom we are more closely related, including those species (usually terrestrial) to whom we refer as charismatic megafauna. Many of my examples come from animals that are more well studied but they can be used as models for aquatic animals. I follow Darwinian notions of evolutionary continuity to argue that if we feel pain, then so too do many other animals, including those that live in aquatic environs. Recent scientific data ('science sense') show clearly that many aquatic organisms, much to some people's surprise, likely suffer at our hands and feel their own sorts of pain. Throughout I discuss how cognitive ethology (the study of animal minds) is the unifying science for understanding the subjective, emotional, empathic, and moral lives of animals because it is essential to know what animals do, think, and feel as they go about their daily routines. Lastly, I argue that when we are uncertain if we are inflicting pain due to our incessant, annoying, and frequently unnecessary intrusions into the lives of other animals as we go about 'redecorating nature' (removing animals or moving them from place to place), we should err on the side of the animals and stop engaging in activities that cause pain and suffering.     

Animal welfare and the refinement of neuroscience research methods--a case study of Huntington's disease models

The use of animals in biomedical and other research presents an ethical dilemma: we do not want to lose scientific benefits, nor do we want to cause laboratory animals to suffer. Scientists often refer to the potential human benefits of animal models to justify their use. However, even if this is accepted, it still needs to be argued that the same benefits could not have been achieved with a mitigated impact on animal welfare. Reducing the adverse effects of scientific protocols ('refinement') is therefore crucial in animal-based research. It is especially important that researchers share knowledge on how to avoid causing unnecessary suffering. We have previously demonstrated that even in studies in which animal use leads to spontaneous death, scientists often fail to report measures to minimize animal distress (Olsson et al. 2007). In this paper, we present the full results of a case study examining reports, published in peer-reviewed journals between 2003 and 2004, of experiments employing animal models to study the neurodegenerative disorder Huntington's disease. In 51 references, experiments in which animals were expected to develop motor deficits so severe that they would have difficulty eating and drinking normally were conducted, yet only three references were made to housing adaptation to facilitate food and water intake. Experiments including end-stages of the disease were reported in 14 papers, yet of these only six referred to the euthanasia of moribund animals. If the reference in scientific publications reflects the actual application of refinement, researchers do not follow the 3Rs (replacement, reduction, refinement) principle. While in some cases, it is clear that less-than-optimal techniques were used, we recognize that scientists may apply refinement without referring to it; however, if they do not include such information in publications, it suggests they find it less relevant. Journal publishing policy could play an important role: first, in ensuring that referees seriously consider whether submitted studies were indeed carried out with the smallest achievable negative impact on the animals and, secondly, in encouraging scientists to share refinements through the inclusion of a 3Rs section in papers publishing the results of animal-based research.     

Current issues in fish welfare

Human beings may affect the welfare of fish through fisheries, aquaculture and a number of other activities. There is no agreement on just how to weigh the concern for welfare of fish against the human interests involved, but ethical frameworks exist that suggest how this might be approached. Different definitions of animal welfare focus on an animal's condition, on its subjective experience of that condition and/or on whether it can lead a natural life. These provide different, legitimate, perspectives, but the approach taken in this paper is to focus on welfare as the absence of suffering. An unresolved and controversial issue in discussions about animal welfare is whether non‐human animals exposed to adverse experiences such as physical injury or confinement experience what humans would call suffering. The neocortex, which in humans is an important part of the neural mechanism that generates the subjective experience of suffering, is lacking in fish and non‐mammalian animals, and it has been argued that its absence in fish indicates that fish cannot suffer. A strong alternative view, however, is that complex animals with sophisticated behaviour, such as fish, probably have the capacity for suffering, though this may be different in degree and kind from the human experience of this state. Recent empirical studies support this view and show that painful stimuli are, at least, strongly aversive to fish. Consequently, injury or experience of other harmful conditions is a cause for concern in terms of welfare of individual fish. There is also growing evidence that fish can experience fear‐like states and that they avoid situations in which they have experienced adverse conditions. Human activities that potentially compromise fish welfare include anthropogenic changes to the environment, commercial fisheries, recreational angling, aquaculture, ornamental fish keeping and scientific research. The resulting harm to fish welfare is a cost that must be minimized and weighed against the benefits of the activity concerned. Wild fish naturally experience a variety of adverse conditions, from attack by predators or conspecifics to starvation or exposure to poor environmental conditions. This does not make it acceptable for humans to impose such conditions on fish, but it does suggest that fish will have mechanisms to cope with these conditions and reminds us that pain responses are in some cases adaptive (for example, suppressing feeding when injured). In common with all vertebrates, fish respond to environmental challenges with a series of adaptive neuro‐endocrine adjustments that are collectively termed the stress response. These in turn induce reversible metabolic and behavioural changes that make the fish better able to overcome or avoid the challenge and are undoubtedly beneficial, in the short‐term at least. In contrast, prolonged activation of the stress response is damaging and leads to immuno‐suppression, reduced growth and reproductive dysfunction. Indicators associated with the response to chronic stress (physiological endpoints, disease status and behaviour) provide a potential source of information on the welfare status of a fish. The most reliable assessment of well‐being will be obtained by examining a range of informative measures and statistical techniques are available that enable several such measures to be combined objectively. A growing body of evidence tells us that many human activities can harm fish welfare, but that the effects depend on the species and life‐history stage concerned and are also context‐dependent. For example, in aquaculture, adverse effects related to stocking density may be eliminated if good water quality is maintained. At low densities, bad water quality may be less likely to arise whereas social interactions may cause greater welfare problems. A number of key differences between fish and birds and mammals have important implications for their welfare. Fish do not need to fuel a high body temperature, so the effects of food deprivation on welfare are not so marked. For species that live naturally in large shoals, low rather than high densities may be harmful. On the other hand, fish are in intimate contact with their environment through the huge surface area of their gills, so they are vulnerable to poor water quality and water borne pollutants. Extrapolation between taxa is dangerous and general frameworks for ensuring welfare in other vertebrate animals need to be modified before they can be usefully applied to fish. The scientific study of fish welfare is at an early stage compared with work on other vertebrates and a great deal of what we need to know is yet to be discovered. It is clearly the case that fish, though different from birds and mammals, however, are sophisticated animals, far removed from unfeeling creatures with a 15 s memory of popular misconception. A heightened appreciation of these points in those who exploit fish and in those who seek to protect them would go a long way towards improving fish welfare.     

A user's guide to animal welfare science

Here, I provide a guide for those new to the burgeoning field of animal welfare science as to what this comprehensive, relatively young discipline is all about. Drawing on all branches of biology, including behavioural ecology and neuroscience, the science of animal welfare asks three big questions: Are animals conscious? How can we assess good and bad welfare in animals? How can we use science to improve animal welfare in practice? I also provide guidelines for an evidence-based approach to welfare issues for policy makers and other users of animal welfare research.     

Uncertainties about 'painless' animals

Macer explores whether it is possible to genetically alter animals to reduce or eliminate their capacity to feel pain, whether it would be ethical to do so, and how we would regard animals that do not feel pain. A possible use for such animals would be as subjects for laboratory research. Among the scientific, philosophical, and ethical uncertainties of pain that Macer considers are: can we define pain? how do we measure pain and anxiety? is pain always related to suffering? what is the minimum level of pain that a being must be able to feel before we reach the conclusion that it should not be used by other beings? are we justified in using beings that do not feel pain when we would not be if they did feel pain and suffer from it?     

Concepts of Animal Welfare in Relation to Positions in Animal Ethics

When animal ethicists deal with welfare they seem to face a dilemma: On the one hand, they recognize the necessity of welfare concepts for their ethical approaches. On the other hand, many animal ethicists do not want to be considered reformist welfarists. Moreover, animal welfare scientists may feel pressed by moral demands for a fundamental change in our attitude towards animals. The analysis of this conflict from the perspective of animal ethics shows that animal welfare science and animal ethics highly depend on each other. Welfare concepts are indispensable in the whole field of animal ethics. Evidence for this can be found by analyzing the structure of theories of animal ethics and the different ways in which these theories employ welfare concepts. Furthermore, the background of values underneath every welfare theory is essential to pursue animal welfare science. Animal ethics can make important contributions to the clarification of underlying normative assumptions with regard to the value of the animal, with regard to ideas about what is valuable for the animal, and with regard to the actions that should follow from the results of animal welfare science.     

Genetically modified laboratory animals--what welfare problems do they face?

In this article, we respond to public concern expressed about the welfare of genetically modified (GM) nonhuman animals. As a contribution to the debate on this subject, we attempt in this article to determine in what situations the practice of genetic modification in rodents may generate significant welfare problems. After a brief discussion of the principles of animal welfare, we focus on the problem of animal suffering and review some types of gene modifications likely to cause predictable welfare problems. In this article, we also consider suffering that may be involved in the process of generating GM animals. Finally, we discuss the role of GM animals in attempts to reduce, replace, and refine the use of animals in research.     

Reflecting on ethical and legal issues in wildlife disease

Disease in wildlife raises a number of issues that have not been widely considered in the bioethical literature. However, wildlife disease has major implications for human welfare. The majority of emerging human infectious diseases are zoonotic: that is, they occur in humans by cross‐species transmission from animal hosts. Managing these diseases often involves balancing concerns with human health against animal welfare and conservation concerns. Many infectious diseases of domestic animals are shared with wild animals, although it is often unclear whether the infection spills over from wild animals to domestic animals or vice versa. Culling is the standard means of managing such diseases, bringing economic considerations, animal welfare and conservation into conflict. Infectious diseases are also major threatening processes in conservation biology and their appropriate management by culling, vaccination or treatment raises substantial animal ethics issues. One particular issue of great significance in Australia is an ongoing research program to develop genetically modified pathogens to control vertebrate pests including rabbits, foxes and house mice. Release of any self‐replicating GMO vertebrate pathogen gives rise to a whole series of ethical questions. We briefly review current Australian legal responses to these problems. Finally, we present two unresolved problems of general importance that are exemplified by wildlife disease. First, to what extent can or should ‘bioethics’ be broadened beyond direct concerns with human welfare to animal welfare and environmental welfare? Second, how should the irreducible uncertainty of ecological systems be accounted for in ethical decision making?     

Towards welfare biology: Evolutionary economics of animal consciousness and suffering

Welfare biology is the study of living things and their environment with respect to their welfare (defined as net happiness, or enjoyment minus suffering). Despite difficulties of ascertaining and measuring welfare and relevancy to normative issues, welfare biology is a positive science. Evolutionary economics and population dynamics are used to help answer basic questions in welfare biology: Which species are affective sentients capable of welfare? Do they enjoy positive or negative welfare? Can their welfare be dramatically increased? Under plausible axioms, all conscious species are plastic and all plastic species are conscious (and, with a stronger axiom, capable of welfare). More complex niches favour the evolution of more rational species. Evolutionary economics also supports the common-sense view that individual sentients failing to survive to mate suffer negative welfare. A kind of God-made (or evolution-created) fairness between species is also unexpectedly found. The contrast between growth maximization (as may be favoured by natural selection), average welfare, and total welfare maximization is discussed. It is shown that welfare could be increased without even sacrificing numbers (at equilibrium). Since the long-term reduction in animal suffering depends on scientific advances, strict restrictions on animal experimentation may be counter-productive to animal welfare.     

Cognitive ability and sentience: which aquatic animals should be protected?

It is of scientific and practical interest to consider the levels of cognitive ability in animals, which animals are sentient, which animals have feelings such as pain and which animals should be protected. A sentient being is one that has some ability to evaluate the actions of others in relation to itself and third parties, to remember some of its own actions and their consequences, to assess risk, to have some feelings and to have some degree of awareness. These abilities can be taken into account when evaluating welfare. There is evidence from some species of fish, cephalopods and decapod crustaceans of substantial perceptual ability, pain and adrenal systems, emotional responses, long- and short-term memory, complex cognition, individual differences, deception, tool use, and social learning. The case for protecting these animals would appear to be substantial. A range of causes of poor welfare in farmed aquatic animals is summarised.     

Attitudes of Dairy Farmers toward Cow Welfare in Relation to Housing,Management and Productivity

ABSTRACT

The quality of stockmanship contributes to the human–animal relationship, animal welfare and productivity. Attitudes can affect the way farmers treat their animals, the environment they provide the animals with, and even their own job satisfaction through the feedback received from the animals. Farmers' perceptions of animals have also been shown to have an impact on productivity. We investigated 161 Finnish dairy farmers' attitudes toward improving animal welfare through an attitude questionnaire that used the Theory of Planned Behavior as a theoretical framework. The theory states that personal attitude, subjective norms, and perceived behavioral control, together shape an individual's behavioral intentions and behaviors. To study the relationship between attitudes, animal welfare, and milk production, we used environment-based animal welfare indicator data consisting of categorized housing and management parameters, and mean milk production data. Non-parametric partial correlation analyses and regression analyses revealed that perceiving the measures to improve animal welfare to be important and easy were positively, although weakly, related to higher animal welfare standards/indicators, while no connection with production was established. Contrary to our expectations, sources of subjective norms, such as an agricultural adviser, were mostly negatively linked with animal welfare indicators and even with production. The farmers considered taking care of their own well-being as the most important way of improving animal welfare, and intending to do so was weakly but positively linked with animal welfare indicators. Any causal relationships, however, cannot be derived from the data.     

Expanding the moral circle: farmed fish as objects of moral concern

Until recently fish welfare attracted little attention, but international and national legislation and standards of fish welfare are now emerging and an overview of these developments is presented in this study. Whereas animal welfare legislation is based on public morality, animal ethics does not automatically accept public morality as normative and elaborates arguments regarding the way humans should treat animals (referred to as moral standards). In this study we present the most common animal ethics theories. For most of these, sentience is considered a demarcation line for moral concern: if an animal is sentient, then it should be included in the moral circle, i.e. receive moral consideration in its own right and some basic welfare should be ensured. As for fish, research has revealed that the sensory system of teleosts can detect noxious stimuli, and that some kind of phenomenal consciousness, allowing the fish to feel pain, seems to be present. This raises the ethical question as to how much evidence we need in order to act on such indications of fish sentience. A simple risk analysis shows that the probability that fishes can feel pain is not negligible and that if they do indeed experience pain the consequences in terms of the number of suffering individuals are great. We conclude that farmed fish should be given the benefit of the doubt and we should make efforts that their welfare needs are met as well as possible. Finally, the way forward is briefly discussed: efforts must be made to understand what fish welfare means in practical fish farming. This will involve the development of research and education, greater accountability and transparency, compliance with and control of policies, and quality assurance schemes.     

Agitated honeybees exhibit pessimistic cognitive biases

Whether animals experience human-like emotions is controversial and of immense societal concern [1-3]. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures [4-8]. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes [9-11]. Recently, mammals [12-16] and birds [17-20] with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, we ask whether honeybees display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. We show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, we show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions.     

Low Levels of Empathic Concern Predict Utilitarian Moral Judgment

Is it permissible to harm one to save many? Classic moral dilemmas are often defined by the conflict between a putatively rational response to maximize aggregate welfare (i.e., the utilitarian judgment) and an emotional aversion to harm (i.e., the non-utilitarian judgment). Here, we address two questions. First, what specific aspect of emotional responding is relevant for these judgments? Second, is this aspect of emotional responding selectively reduced in utilitarians or enhanced in non-utilitarians? The results reveal a key relationship between moral judgment and empathic concern in particular (i.e., feelings of warmth and compassion in response to someone in distress). Utilitarian participants showed significantly reduced empathic concern on an independent empathy measure. These findings therefore reveal diminished empathic concern in utilitarian moral judges.