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.     

Fish research and the institutional animal care and use committee

Fish represent the most diverse group of animals in the vertebrate phylum. The more than 25,000 species are characterized by an array of anatomical, biochemical, physiological, and behavioral repertoires. For this reason, it is difficult to develop a comprehensive guideline on the care and use of fishes. Institutional animal care and use committees (IACUCs) meet the challenge of ensuring adequate fish welfare using guidelines (Animal Welfare Act [AWA] and Public Health Service [PHS] Policy and their guides) derived mainly from the care and use of mammalian species, which may not be optimal for regulating fish research, teaching, or extension activities. Discussion focuses on various issues that often confront IACUCs in meeting regulatory requirements while assuring proper fish welfare. Issues include questions concerning animal tracking and inventory, utilization of fisheries bycatch, facility inspections in remote locations, and euthanasia. Common sense solutions appropriate for field and laboratory fish activities are suggested, which should help investigators, IACUCs, and regulatory agencies meet PHS and AWA objectives.     

The Controversy on Fish Pain: A Veterinarian’s Perspective

Fish welfare is still a relatively new field. As such, regulations and protocols to ensure fish welfare are currently limited and vary considerably in different jurisdictions. This is in part because of the ongoing controversy as to whether or not fish feel pain. This controversy has persisted for several years, yet veterinarians have been mostly absent from the discussion so far. This essay aims to address this issue. Here, it is argued that while this controversy has its place, it is unlikely to be resolved in the near future. Fish welfare could instead be improved by pursuing more clinically applicable research to increase knowledge of fishes’ behavior and physiology. Such research would assist in learning the optimal environment for their specific needs, as well as compiling some verified indicators of pain in fish. This would then lead to improved studies that could help to determine if and when analgesic drugs can be beneficial in fish, as they are in many other species.     

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.     

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.     

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.     

High species richness of early stages of fish in a locality of the Mesoamerican Barrier Reef System: a small-scale survey using different sampling gears

The Mesoamerican Barrier Reef System (MBRS) contains a diverse array of coastal habitats that are critical for the survival of the early stages of reef fish; however, the knowledge on the abundance and distribution of the early stages of coastal fishes is still limited in this region. This study investigated the species richness of larval and juvenile fishes using a combination of a sled net, standard plankton net, and a nightlight lift-net; these were deployed simultaneously at Bacalar Chico, a site on the MBRS within the protected “Parque Nacional Arrecifes de Xcalak” (PNAX). We collected 53 families and 118 species of larval and juvenile fishes in a small area of about 3 km². This species diversity of early life-history stages is greater than previously found in surveys on the MBRS. Each gear caught a number of species exclusively, so combined sampling with the three methods provided a much fuller picture of the local larval and juvenile fish assemblage. A species-accumulation model estimated that the samples likely represented 84% of the total assemblage. Many species caught were represented predominantly by newly settled juveniles, underscoring the importance of this coastal habitat for settlement of many ecologically and economically important fish species. This information is expected to improve the conservation and management strategies in the fragile PNAX coastal zones by providing additional information based on original field data to raise awareness among managers about the ecological relevance of these coastal habitats. This study provides encouraging evidence that the PNAX is a well-suited natural protected area to preserve a critical fish habitat in a hotspot of marine biodiversity.     

Variability of the behavioral laterality in Teleostei (Pisces)

Factors causing variability of behavioral laterality in Teleostei are reviewed. The laterality has been revealed in many fish species belonging to various families. The best ever demonstrated example of the laterality is the different use of the right and left eyes when a fish responds to different visual objects. Magnitude and sign of the laterality differ in fishes of different species, gender, and age. Also, an observed laterality depends on how familiar a stimulus is to fishes and what it means to them, as well as their motivational level and various behavioral traits. Therefore, comparisons of the laterality among different fish species should be based on experimental methods that also take into account those behavioral differences among them that are not directly linked to the laterality.     

Stress and welfare in ornamental fishes: what can be learned from aquaculture?

The ornamental fish trade is estimated to handle up to 1·5 billion fishes. Transportation and handling of fishes imposes a range of stressors that can result in mortality at rates of up to 73%. These rates vary hugely, however, and can be as low as 2%, because they are generally estimated rather than based on experimental work. Given the numbers of ornamental fishes traded, any of the estimated mortality rates potentially incur significant financial losses and serious welfare issues. Industry bodies, such as the Ornamental Aquatic Trade Association (OATA), have established standards and codes of best practice for handling fishes, but little scientific research has been conducted to understand the links between stress, health and welfare in ornamental species. In aquaculture, many of the same stressors occur as those in the ornamental trade, including poor water quality, handling, transportation, confinement, poor social and physical environment and disease and in this sector directed research and some resulting interventions have resulted in improved welfare standards. This review considers the concept of welfare in fishes and evaluates reported rates of mortality in the ornamental trade. It assesses how the stress response can be quantified and used as a welfare indicator in fishes. It then analyses whether lessons from aquaculture can be usefully applied to the ornamental fish industry to improve welfare. Finally, this analysis is used to suggest how future research might be directed to help improve welfare in the ornamental trade.     

Candidatus Syngnamydia Venezia,a Novel Member of the Phylum Chlamydiae from the Broad Nosed Pipefish,Syngnathus typhle

Chlamydia are obligate intracellular bacteria and important pathogens of humans and animals. Chlamydia-related bacteria are also major fish pathogens, infecting epithelial cells of the gills and skin to cause the disease epitheliocystis. Given the wide distribution, ancient origins and spectacular diversity of bony fishes, this group offers a rich resource for the identification and isolation of novel Chlamydia. The broad-nosed pipefish (Syngnathus typhle) is a widely distributed and genetically diverse temperate fish species, susceptible to epitheliocystis across much of its range. We describe here a new bacterial species, Candidatus Syngnamydia venezia; epitheliocystis agent of S. typhle and close relative to other chlamydial pathogens which are known to infect diverse hosts ranging from invertebrates to humans.     

Behavioral Isolation Based on Visual Signals in a Sympatric Pair of Darter Species

Elaborate visual communication signals characterize many animal lineages. Often sex‐limited, these signals are generally assumed to result from sexual selection, and in many cases, their evolution is thought to play a central role in speciation. The co‐evolution of male visual signals and female preferences is hypothesized to result in behavioral isolation between divergent lineages; however, for many lineages characterized by elaborate visual signals, the importance of visual differences in behavioral isolation is not well established. Darters (fish genus Etheostoma) are particularly appropriate for examining the role of visual signals in behavioral isolation. They comprise one of the most diverse groups of North American freshwater fish, and nearly every species is characterized by unique nuptial coloration. Multiple darter species co‐exist in sympatric populations, indicating that reproductive barriers are central to maintaining these extraordinarily diverse color patterns. This study demonstrates the presence of behavioral isolation between a pair of distinctly colored sympatric darter species, Etheostoma barrenense and Etheostoma zonale, through experimental observations using an artificial stream. In addition, a series of dichotomous mate‐choice trials indicate that females prefer conspecific males over heterospecifics based on visual differences alone. We therefore provide the first evidence that visual signals are a critical trait maintaining behavioral isolation in darters, a lineage of fishes with spectacular diversification in visual communication.     

Intestinal microbiota composition in fishes is influenced by host ecology and environment

The digestive tracts of vertebrates are colonized by complex assemblages of micro-organisms, collectively called the gut microbiota. Recent studies have revealed important contributions of gut microbiota to vertebrate health and disease, stimulating intense interest in understanding how gut microbial communities are assembled and how they impact host fitness (Sekirov et al. 2010). Although all vertebrates harbour a gut microbiota, current information on microbiota composition and function has been derived primarily from mammals. Comparisons of different mammalian species have revealed intriguing associations between gut microbiota composition and host diet, anatomy and phylogeny (Ley et al. 2008b). However, mammals constitute <10% of all vertebrate species, and it remains unclear whether similar associations exist in more diverse and ancient vertebrate lineages such as fish. In this issue, Sullam et al. (2012) make an important contribution toward identifying factors determining gut microbiota composition in fishes. The authors conducted a detailed meta-analysis of 25 bacterial 16S rRNA gene sequence libraries derived from the intestines of different fish species. To provide a broader context for their analysis, they compared these data sets to a large collection of 16S rRNA gene sequence data sets from diverse free-living and host-associated bacterial communities. Their results suggest that variation in gut microbiota composition in fishes is strongly correlated with species habitat salinity, trophic level and possibly taxonomy. Comparison of data sets from fish intestines and other environments revealed that fish gut microbiota compositions are often similar to those of other animals and contain relatively few free-living environmental bacteria. These results suggest that the gut microbiota composition of fishes is not a simple reflection of the micro-organisms in their local habitat but may result from host-specific selective pressures within the gut (Bevins & Salzman 2011).     

Identifying and monitoring pain in farm animals: a review

One important objective for animal welfare is to maintain animals free from pain, injury or disease. Therefore, detecting and evaluating the intensity of animal pain is crucial. As animals cannot directly communicate their feelings, it is necessary to identify sensitive and specific indicators that can be easily used. The aim of the present paper is to review relevant indicators to assess pain in several farm species. The term pain is used for mammals, birds and fish, even though the abilities of the various species to experience the emotional component of pain may be different. Numerous behavioural changes are associated with pain and many of them could be used on farms to assess the degree of pain being experienced by an animal. Pain, as a stressor, is associated with variations in the hypothalamic–pituitary–adrenal axis as well as in the sympathetic and immune systems that can be used to identify the presence of pain rapidly after it started. However, most of these measures need sophisticated equipment for their assessment. Therefore, they are mainly adapted to experimental situations. Injuries and other lesional indicators give information on the sources of pain and are convenient to use in all types of situations. Histopathological analyses can identify sources of pain in experimental studies. When pronounced and/or long lasting, the pain-induced behavioural and physiological changes can decrease production performance. Some indicators are very specific and sensitive to pain, whereas others are more generally related to stressful situations. The latter can be used to indicate that animals are suffering from something, which may be pain. Overall, this literature review shows that several indicators exist to assess pain in mammals, a few in birds and very few in fish. Even if in some cases, a single indicator, usually a behavioural indicator, may be sufficient to detect pain, combining various types of indicators increases sensitivity and specificity of pain assessment. Research is needed to build and validate new indicators and to develop systems of pain assessment adapted to each type of situation and each species.     

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.     

Freshwater fish introductions in Spain: facts and figures at the beginning of the 21st century

Twenty-five introduced fish species are established in Spanish fresh waters. Most of the introductions took place after 1900, with a significant exponential increase during the second half of the 20th century (15 species introduced from 1949). Major stocking efforts in Spanish waters have been suspended, but recently some species have been released by anglers or are suspected to be escapes from fish farms. Stream regulation is considered to be one of the main negative factors affecting river ecosystems in Spain, but many of the aliens adapt well to these altered habitats. Competition between native and exotic fishes is certain to occur to some degree, but there is little quantitative information. Fish conservation and fishery management must not be based on the 'introduce anything' sentiment that has developed over more than a century. Information, education and public awareness are critical components of any effort to prevent the spread of introduced fish species.     

Belief in Animal Mind among Spanish Primary School Children

Beliefs concerning the mental experiences of nonhuman animals have been related to how people treat, see, and take care of nonhuman animals. Whereas this issue has been the subject of several studies on adults, few have been conducted with children. Taking advantage of a recently published scale, the Child-BAM questionnaire, we aimed to explore the beliefs in animal minds of Spanish primary school children. The study also considered the effects of a child's age, school year group, gender, and pet ownership on their beliefs in animal mind. The Child-BAM questionnaire, concerning the mental capabilities of eight different species (human, chimpanzee, dog, cow, otter, sparrow, frog, and fish), was distributed at a primary school sited in Cordoba, Spain. A total of 416 participants were included aged between 6 and 13 years. Each child provided scores for animals’ ability to have intelligence, experience pain, fear, happiness, and sadness, and total scores for the eight species were calculated. The results showed that children's beliefs about animal minds differed depending on the type of animal, and that children were more likely to believe in the emotional capacities of animals rather than their cognitive capabilities. Dogs achieved similar scores to humans regarding all capabilities, and higher than any other species, while the cow, fish, and frog generally scored the lowest. Age, school year group, and having a companion animal at home affected beliefs in animal minds, whereas gender had no effect. This study highlights cultural similarities in children's beliefs about animal minds and the potential importance of this variable for future research in child–animal interactions.     

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.     

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.     

无意识接受策略在挫折情景下的情绪调节效应:行为与生理证据

由于无意识调节过程具有节省认知资源的特征,本研究假设无意识接受策略相比有意识接受策略能更加有效地调控负性事件的情绪影响.实验以挫折任务诱发负面情绪同时记录被试的主观情绪体验与情绪相关的生理变化(心率).被试被随机分为控制组、有意识接受组和无意识接受组.结果显示,无意识接受组和有意识接受组在情绪体验上存在显著差异:在挫折诱发阶段有意识接受组比无意识接受组出现了更多正性情绪指标的下降.此外,相对于控制组,挫折情景下有意识接受和无意识接受都显著降低了被试情绪相关的心率活动水平;但两者的调节水平无显著差异.并且,心率活动水平可预测主观情绪体验强度:控制组的心率变化值与负性情绪变化值存在正相关关系,与正性情绪指标变化值存在负相关趋势.因此,在挫折情景下,无意识接受策略不仅能有效降低情绪相关的生理活动水平,且相比有意识接受策略对主观情绪体验具有更好的调节效果.这提示,无意识接受策略对于现实生活中的情绪调节具有重要启示意义.