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.     

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.     

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.     

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.     

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.     

Intestinal barrier function of Atlantic salmon (<Emphasis Type="Italic">Salmo salar</Emphasis> L.) post smolts is reduced by common sea cage environments and suggested as a possible physiological welfare indicator

Background  

Fish farmed under high intensity aquaculture conditions are subjected to unnatural environments that may cause stress. Therefore awareness of how to maintain good health and welfare of farmed fish is important. For Atlantic salmon held in sea cages, water flow, dissolved oxygen (DO) levels and temperature will fluctuate over time and the fish can at times be exposed to detrimentally low DO levels and high temperatures. This experimental study investigates primary and secondary stress responses of Atlantic salmon post smolts to long-term exposure to reduced and fluctuating DO levels and high water temperatures, mimicking situations in the sea cages. Plasma cortisol levels and cortisol release to the water were assessed as indicators of the primary stress response and intestinal barrier integrity and physiological functions as indicators of secondary responses to changes in environmental conditions.     

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.     

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.     

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.     

Stress-associated impacts of short-term holding on fishes

Most sources of stress in aquaculture, fish salvage, stocking programs, and commercial and sport fisheries may be unavoidable. Collecting, handling, sorting, holding, and transporting are routine practices that can have significant effects on fish physiology and survival. Nevertheless, an understanding of the stressors affecting fish holding can lead to practices that reduce stress and its detrimental effects. The stress-related effects of short-term holding are influenced by water quality, confinement density, holding container design, and agonistic and predation-associated behaviors. Physiological demands (e.g., resulting from confinement-related stresses) exceeding a threshold level where the fish can no longer compensate may lead to debilitating effects. These effects can be manifested as suppressed immune systems; decreased growth, swimming performance, or reproductive capacity; even death. Furthermore, holding tolerance may depend upon the species, life stage, previous exposure to stress, and behavior of the held fish. Water quality is one of the most important contributors to fish health and stress level. Fish may be able to tolerate adverse water quality conditions; however, when combined with other stressors, fish may be quickly overcome by the resulting physiological challenges. Temperature, dissolved oxygen, ammonia, nitrite, nitrate, salinity, pH, carbon dioxide, alkalinity, and hardness are the most common water quality parameters affecting physiological stress. Secondly, high fish densities in holding containers are the most common problem throughout aquaculture facilities, live-fish transfers, and fish salvage operations. Furthermore, the holding container design may also compromise the survival and immune function by affecting water quality, density and confinement, and aggressive interactions. Lastly, fishes held for relatively short durations are also influenced by negative interactions, associated with intraspecific and interspecific competition, cannibalism, predation, and determining nascent hierarchies. These interactions can be lethal (i.e., predation) or may act as a vector for pathogens to enter (i.e., bites and wounds). Predation may be a significant source of mortality for fisheries practices that do not sort by size or species while holding. Stress associated with short-term holding of fishes can have negative effects on overall health and well-being. These four aspects are major factors contributing to the physiology, behavior, and survival of fishes held for a relatively short time period.     

A review of polymer-based water conditioners for reduction of handling-related injury

Fish are coated with an external layer of protective mucus. This layer serves as the primary barrier against infection or injury, reduces friction, and plays a role in ionic and osmotic regulation. However, the mucus layer is easily disturbed when fish are netted, handled, transported, stressed, or subjected to adverse water conditions. Water additives containing polyvinylpyrrolidone (PVP) or proprietary polymers have been used to prevent the deleterious effects of mucus layer disturbances in the commercial tropical fish industry, aquaculture, and for other fisheries management purposes. This paper reviews research on the effectiveness of water conditioners, and examines the contents and uses of a wide variety of commercially available water conditioners. Water conditioners containing polymers may reduce external damage to fish held in containers during scientific experimentation, including surgical implantation of electronic tags. However, there is a need to empirically test the effectiveness of water conditioners at preventing damage to and promoting healing of the mucus layer. A research agenda is provided to advance the science related to the use of water conditions to improve the condition of fish during handling and tagging.     

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.     

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.     

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.     

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.     

Stunning fish with CO2 or electricity: contradictory results on behavioural and physiological stress responses

Studies that address fish welfare before slaughter have concluded that many of the traditional systems used to stun fish including CO₂ narcosis are unacceptable as they cause avoidable stress before death. One system recommended as a better alternative is electrical stunning, however, the welfare aspects of this method are not yet fully understood. To assess welfare in aquaculture both behavioural and physiological measurements have been used, but few studies have examined the relationship between these variables. In an on-site study aversive behaviours and several physiological stress indicators, including plasma levels of cortisol and ions as well as blood physiological variables, were compared in Arctic char (Salvelinus alpinus) stunned with CO₂ or electricity. Exposure to water saturated with CO₂ triggered aversive struggling and escape responses for several minutes before immobilization, whereas in fish exposed to an electric current immobilization was close to instant. On average, it took 5 min for the fish to recover from electrical stunning, whereas fish stunned with CO₂ did not recover. Despite this, the electrically stunned fish had more than double the plasma levels of cortisol compared with fish stunned with CO₂. This result is surprising considering that the behavioural reactions were much more pronounced following CO₂ exposure. These contradictory results are discussed with regard to animal welfare and stress physiological responses. The present results emphasise the importance of using an integrative and interdisciplinary approach and to include both behavioural and physiological stress indicators in order to make accurate welfare assessments of fish in aquaculture.