Taking account of fish welfare: lessons from aquaculture

This paper explores the possibility that lessons learned from aquaculture might contribute to current debate on welfare and fisheries. After looking briefly at the history of research interest in the welfare of farmed fishes, some implications of using different definitions of and approaches to the concept of welfare are discussed. Consideration is given to the way in which the aquaculture industry has responded to public concern about fish welfare and, for cases where these responses have been effective, why this might be the case. Finally, possible cross‐over points between aquaculture and fisheries in the context of fish welfare, as well as experience and expertise that might be shared between these two areas, are identified.     

The welfare of fish

Our interactions with fish cover a wide range of activities including enjoying them as pets to consuming them as food. I propose that we confine the consideration of the welfare of fish to their physiology, and not join the discussion on whether fish can feel pain and suffering, as humans. A significant proportion of the papers on animal welfare center on whether non-human animals can feel pain, and suffer as humans. This is a question that never can be answered unequivocally. The premise of the present paper is that we have an ethical responsibility to respect the life and wellbeing of all organisms. Thus, we should concentrate on the behavioural, physiological, and cellular indicators of their well-being and attempt to minimize a state of stress in the animals that we have in our care or influence.     

Ecology and welfare of aquatic animals in wild capture fisheries

The expansion of commercial aquaculture production has raised awareness of issues relating to the welfare of aquatic animals. The “Five Freedoms” approach to animal welfare was originally devised for farmed terrestrial animals, and has been applied in some countries to aquatic animals reared in aquaculture due to several commonalities inherent within food production systems. There are now moves towards assessing and addressing aquatic animal welfare issues that may arise in wild capture fisheries. However, all “five freedoms” are regularly contradicted in the natural environment, meaning this concept is inappropriate when considering the welfare of aquatic animals in their natural environments. The feelings-based approach to welfare relies on a suffering centered view that, when applied to the natural aquatic environment, requires use of value judgements, cannot encompass scientific uncertainty regarding awareness in fish, elasmobranchs and invertebrates (despite their unquestioned welfare needs), and cannot resolve the welfare conundrums posed by predator–prey interactions or anthropocentrically mediated environmental degradation. For these reasons, the feelings-based approach to welfare is inadequate, inappropriate and must be rejected if applied to aquatic animals in wild capture fisheries, because it demonstrably ignores empirical evidence and several realities apparent within the natural aquatic environment. Furthermore, application of the feelings-based approach is counterproductive as it can alienate key fisheries stakeholders, many of whom are working to address environmental issues of critical importance to the welfare, management and conservation of aquatic animal populations in their natural environment. In contrast, the function-based and nature-based approaches for defining animal welfare appear appropriate for application to the broad range of welfare issues (including emerging environmental issues such as endocrine disruption) that affect aquatic animals in their natural environment, without the need to selectively ignore groups such as elasmobranchs and invertebrates. We consider that the welfare needs of aquatic animals are inextricably entwined with the need for conservation of their populations, communities and their environment, an approach that is entirely consistent with the concept of ecosystem-based management.     

The ethics of fish welfare

The topic of fish welfare in the context of commercial fisheries is a difficult one. From traditionally anthropocentric or human‐centred perspectives, fishes are simply objects for humans to use as they see fit. When it is argued that anthropocentrism is arbitrary, it may appear that a strong animal rights position is the only recourse, with the result that humans ought not to use animals in the first place, if it is at all possible. It can be argued that both positions fail to view human beings as part of the natural world. If human beings are viewed as part of the world from which they live, then it has to be asked what it means to be respectful of the animals which humans use and from which they live. From this perspective, concern for the welfare of the fishes humans eat is simply what should be expected from humans as good citizens in the community of living creatures.     

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.     

Cumulative stress in research animals: Telomere attrition as a biomarker in a welfare context?

Progress in improving animal welfare is currently limited by the lack of objective methods for assessing lifetime experience. I propose that telomere attrition, a cellular biomarker of biological age, provides a molecular measure of cumulative experience that could be used to assess the welfare impact of husbandry regimes and/or experimental procedures on non‐human animals. I review evidence from humans that telomere attrition is accelerated by negative experiences in a cumulative and dose‐dependent manner, but that this attrition can be mitigated or even reversed by positive life‐style interventions. Evidence from non‐human animals suggests that despite some specific differences in telomere biology, stress‐induced telomere attrition is a robust phenomenon, occurring in a range of species including mice and chickens. I conclude that telomere attrition apparently integrates positive and negative experience in an accessible common currency that translates readily to novel species – the Holy Grail of a cumulative welfare indicator.     

The Science of Animal Suffering

Can suffering in non‐human animals be studied scientifically? Apart from verbal reports of subjective feelings, which are uniquely human, I argue that it is possible to study the negative emotions we refer to as suffering by the same methods we use in ourselves. In particular, by asking animals what they find positively and negatively reinforcing (what they want and do not want), we can define positive and negative emotional states. Such emotional states may or may not be accompanied by subjective feelings but fortunately it is not necessary to solve the problem of consciousness to construct a scientific study of suffering and welfare. Improvements in animal welfare can be based on the answers to two questions: Q1: Will it improve animal health? and Q2: Will it give the animals something they want? This apparently simple formulation has the advantage of capturing what most people mean by ‘improving welfare’ and so halting a potentially dangerous split between scientific and non‐scientific definitions of welfare. It can also be used to validate other controversial approaches to welfare such as naturalness, stereotypies, physiological and biochemical measures. Health and what animals want are thus not just two of many measures of welfare. They provide the definition of welfare against which others can be validated. They also tell us what research we have to do and how we can judge whether welfare of animals has been genuinely improved. What is important, however, is for this research to be done in situ so that it is directly applicable to the real world of farming, the sea or an animal’s wild habitat. It is here that ethology can make major contributions.     

Review: Assessing fish welfare in research and aquaculture,with a focus on European directives

The number of farmed fish in the world has increased considerably. Aquaculture is a growing industry that will in the future provide a large portion of fishery products. Moreover, in recent years, the number of teleost fish used as animal models for scientific research in both biomedical and ecological fields has increased. Therefore, it is increasingly important to implement measures designed to enhance the welfare of these animals. Currently, a number of European rules exist as requirements for the establishment, care and accommodation of fish maintained for human purposes. As far as (teleost) fish are concerned, the fact that the number of extant species is much greater than that of all other vertebrates must be considered. Of further importance is that each species has its own specific physical and chemical requirements. These factors make it difficult to provide generalized recommendations or requirements for all fish species. An adequate knowledge is required of the physiology and ecology of each species bred. This paper integrates and discusses, in a single synthesis, the current issues related to fish welfare, considering that teleosts are target species for both aquaculture and experimental models in biological and biomedical research. We first focus on the practical aspects, which must be considered when assessing fish welfare in both research and aquaculture contexts. Next, we address husbandry and the care of fish housed in research laboratories and aquaculture facilities in relation to their physiological and behavioural requirements, as well as in reference to the suggestions provided by European regulations. Finally, to evaluate precisely which parameters described by Directive 2010/63/EU are reported in scientific papers, we analysed 82 articles published by European researchers in 2014 and 2015. This review found that there is a general lack of information related to the optimal environmental conditions that should be provided for the range of species covered by this directive.     

Using model selection to choose a size-based condition index that is consistent with operational welfare indicators

Quantitative and qualitative measures of fish health and welfare are essential for management of both wild capture and aquaculture species. These measures include morphometric body condition indices, energetic condition and aquaculture operational welfare indicators (OWIs). Measures vary in ease of measurement (and may require destructive sampling), and it is critical to know how well they correlate with fish health and welfare so appropriate management decisions can be based on them. Lumpfish (Cyclopterus lumpus) is a new farming species that needs nondestructive OWIs to be developed and validated. In this study, we developed a C. lumpus fin damage score. Four different body condition indexes based on individual weight relative to either length–weight relationships or relative to other fish in its local environment were tested (using model selection) as predictors of individual fin damage. Results showed severity of fin damage was predicted by small size relative to the other individuals in the tank or cage. Body condition based on length–weight relationship was not found to predict fin damage, indicating that using established indices from fisheries or from other species would not predict welfare risks from fin damage. Implications are that especially in hatchery conditions grading will improve the condition index, and is expected to mitigate fin damage, but that low weight at length was not of use in predicting fin damage. Model selection to choose between a suite of possible indices proved powerful and should be considered in other applications where an easily measured index is needed to correlate with other health measures.     

Contribution of pathology to laboratory animal welfare

To promote experimental animal welfare, several countries are engaged in establishing local animal research review committees and appointing supervising veterinarians or other experts. However, a number of adverse conditions leading to intercurrent illness or death remains unnoticed or unidentified. Pathological investigation of unexpectedly ill or dead animals proved to be very useful in indicating conditions compromising animal welfare. In addition, such post-mortem findings may be instructive, with respect to welfare, for those involved in experiments with animals.     

Life in the fast lane: Temperature,density and host species impact survival and growth of the fish ectoparasite Argulus foliaceus

With expanding human populations, the food sector has faced constant pressure to sustainably expand and meet global production demands. In aquaculture this frequently manifests in an animal welfare crisis, with fish increasingly farmed under high production, high stress conditions. These intense environments can result in fish stocks having a high susceptibility to infection, with parasites and associated disease one of the main factors limiting industry growth. Prediction of infection dynamics is key to preventative treatment and mitigation. Considering the climatic and technology driven changes facing aquaculture, an understanding of how parasites react across a spectrum of conditions is required. Here we assessed the impact of temperature, infection density and host species on the life history traits of Argulus foliaceus, a common palearctic fish louse, representative of a parasite group problematic in freshwater aquaculture and fisheries worldwide. Temperature significantly affected development, growth and survival; parasites hatched and developed faster at higher temperatures, but also experienced shorter lifespans when maintained off the host. At high temperatures, these parasites will likely experience a short generation time as their life history traits are completed more rapidly. A. foliaceus additionally grew faster on natural hosts and at lower infection densities. Ultimately such results contribute to prediction of population dynamics, aiding development of effective control to improve animal welfare and reduce industry loss.     

Plant‐based oral vaccines against zoonotic and non‐zoonotic diseases

The shared diseases between animals and humans are known as zoonotic diseases and spread infectious diseases among humans. Zoonotic diseases are not only a major burden to livestock industry but also threaten humans accounting for >60% cases of human illness. About 75% of emerging infectious diseases in humans have been reported to originate from zoonotic pathogens. Because antibiotics are frequently used to protect livestock from bacterial diseases, the development of antibiotic‐resistant strains of epidemic and zoonotic pathogens is now a major concern. Live attenuated and killed vaccines are the only option to control these infectious diseases and this approach has been used since 1890. However, major problems with this approach include high cost and injectable vaccines is impractical for >20 billion poultry animals or fish in aquaculture. Plants offer an attractive and affordable platform for vaccines against animal diseases because of their low cost, and they are free of attenuated pathogens and cold chain requirement. Therefore, several plant‐based vaccines against human and animals diseases have been developed recently that undergo clinical and regulatory approval. Plant‐based vaccines serve as ideal booster vaccines that could eliminate multiple boosters of attenuated bacteria or viruses, but requirement of injectable priming with adjuvant is a current limitation. So, new approaches like oral vaccines are needed to overcome this challenge. In this review, we discuss the progress made in plant‐based vaccines against zoonotic or other animal diseases and future challenges in advancing this field.     

Phylogenetic comparative methods: Harnessing the power of species diversity to investigate welfare issues in captive wild animals

This paper reviews a way of investigating health and welfare problems in captive wild animals (e.g., those in zoos, aviaries, aquaria, or aquaculture systems) that has great potential, but to date has been little used: systematically comparing species with few or no health and welfare issues to those more prone to problems. Doing so empirically pinpoints species‐typical welfare risk and protective factors (such as aspects of their natural behavioral biology): information which can then be used to help prevent or remedy problems by suggesting new ways to improve housing and husbandry, and by identifying species intrinsically best suited to captivity. We provide a detailed, step‐by‐step “how to” guide for researchers interested in using these techniques, including guidance on how to statistically control for the inherent similarities shared by related species: an important concern because simple, cross‐species comparisons that do not do this may well fail to meet statistical assumptions of non‐independence. The few relevant studies that have investigated captive wild animals’ welfare problems using this method are described. Overall, such approaches reap value from the great number and diversity of species held in captivity (e.g., the many thousands of species held in zoos); can yield new insights from existing data and published results; render previously intractable welfare questions (such as “do birds need to fly?” or “do Carnivora need to hunt?”) amenable to study; and generate evidence‐based principles for integrating animal welfare into collection planning.     

Domestication and absolute ownership of fish in the English common law

The English common law has, for the purpose of describing the rights of ownership of animals, divided them into two classes, those the subject of absolute ownership and those the subject of a limited property right. In this system, fish have long been regarded as the subject of a limited property right, one dependent on possession.
The principles underlying those concepts follow the Roman law concepts applicable to the proprietorship of animals and adopted in much of Europe. Those principles were further developed and adapted over many centuries in England, but more significantly in the common law countries outside of England, over the last century. They are principles that have a limited relationship to domestication. Drawing on the recent decisions outside of England it is possible to refashion the commonly presented tests as to the absolute ownership of animals. Based on those decisions, it may be asserted, that a person may absolutely own an animal that is a member of a population of animals that have had a long association with humans, or are exploited by a community in a recognized manner, other than by hunting. When applied to fish, particularly those from stock enhancement, sea ranching and aquaculture escapes, those principles raise a number of questions. Does the aquaculturist remain the owner of the fish that have escaped? Is it possible to retain ownership of stock enhancements and sea ranched fish? In some cases they may also raise an issue as to the liability for those fish at large.     

Anthropomorphism and 'mental welfare' of fishes

Anthropomorphism, the use of human characteristics as a foundation for interpreting behavior and mental capacities of animals, is a bias undermining our understanding of other species, especially species as evolutionarily distant from humans as fishes. Anthropomorphism is not justified by allusions to evolutionary continuity among vertebrates, because no living vertebrate was ever a descendant of humans, so none could have inherited human traits. Nonetheless, it has recently been claimed that fishes are capable of conscious experiences of pain and emotional feelings and that mental welfare is an important issue for fishes. This paper shows that the evidence supporting claims for experiences of pain or conscious emotions by fishes is conceptually and methodologically flawed. In addition, the paper shows that the natural history and behavior of diverse fish species is inconsistent with a presumption of human-like awareness. This behavioral evidence is in accord with neurobiological observations showing that fishes are very different from us and are unlikely to have a capacity for awareness of pain or emotional feelings that meaningfully resemble our own. The factors that are detrimental to fish welfare have been well delineated by valid, objective indicators of physiological and behavioral well-being. This knowledge should guide welfare decisions. An empirical and non-anthropomorphic examination of diverse fishes and their adaptations should be the foundation for welfare decisions that would be truly beneficial to fishes and humans alike.     

Ethical considerations in fish research

Fishes are used in a wide range of scientific studies, from conservation research with potential benefits to the species used to biomedical research with potential human benefits. Fish research can take place in both laboratories and field environments and methods used represent a continuum from non-invasive observations, handling, through to experimental manipulation. While some countries have legislation or guidance regarding the use of fish in research, many do not and there exists a diversity of scientific opinions on the sentience of fish and how we determine welfare. Nevertheless, there is a growing pressure on the scientific community to take more responsibility for the animals they work with through maximising the benefits of their research to humans or animals while minimising welfare or survival costs to their study animals. In this review, we focus primarily on the refinement of common methods used in fish research based on emerging knowledge with the aim of improving the welfare of fish used in scientific studies. We consider the use of anaesthetics and analgesics and how we mark individuals for identification purposes. We highlight the main ethical concerns facing researchers in both laboratory and field environments and identify areas that need urgent future research. We hope that this review will help inform those who wish to refine their ethical practices and stimulate thought among fish researchers for further avenues of refinement. Improved ethics and welfare of fishes will inevitably lead to increased scientific rigour and is in the best interests of both fishes and scientists.     

Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments

Many recent papers have deepened the state of knowledge about lactic acid bacteria (LAB) in fish gut. In spite of high variability in fish microbiota, LAB are sometimes abundant in the intestine, notably in freshwater fish. Several strains of Streptococcus are pathogenic to fish. Streptococcus iniae and Lactococcus garvieae are major fish pathogens, against which commercial vaccines are available. Fortunately, most LAB are harmless, and some strains have been reported for beneficial effects on fish health. A major step forward in recent years was the converging evidence that LAB can stimulate the immune system in fish. An open question is whether viability can affect immunostimulation. The issue is crucial to commercialize live probiotics rather than inactivated preparations or extracts. There has been a regain of interest in allochthonous strains used as probiotics for terrestrial animals or humans, due to economical and regulatory constraints, but the short survival in sea water may limit application to marine fish. If viability is required, alternative treatments may include the incorporation of prebiotics in feed, and other dietary manipulations that could promote intestinal LAB. Antagonism to pathogens is the other main feature of candidate probiotics, and there are many reports concerning mainly carnobacteria and Enterococcus. Some bacteriocins were characterized which may be of interest not only for aquaculture, but also for food preservation.     

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.     

The use of probiotics in aquaculture

This study aims to present comprehensive notes for the use of probiotics in aquaculture. Probiotics have been proven to be positive promoters of aquatic animal growth, survival and health. In aquaculture, intestines, gills, the skin mucus of aquatic animals, and habitats or even culture collections and commercial products, can be sources for acquiring appropriate probiotics, which have been identified as bacteria (Gram‐positive and Gram‐negative) and nonbacteria (bacteriophages, microalgae and yeasts). While a bacterium is a pathogen to one aquatic animal, it can bring benefits to another fish species; a screening process plays a significant role in making a probiotic species specific. The administration of probiotics varies from oral/water routine to feed additives, of which the latter is commonly used in aquaculture. Probiotic applications can be either mono or multiple strains, or even in combination with prebiotic, immunostimulants such as synbiotics and synbiotism, and in live or dead forms. Encapsulating probiotics with live feed is a suitable approach to convey probiotics to aquatic animals. Dosage and duration of time are significant factors in providing desired results. Several modes of actions of probiotics are presented, while some others are not fully understood. Suggestions for further studies on the effects of probiotics in aquaculture are proposed.