Rev. sci. tech. Off. int. Epiz., 2014, 33 (1), 233-244
Defining, assessing
and promoting the welfare of farmed fish
F.A. Huntingford (1, 2)* & S. Kadri (2, 3)
(1) Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow,
Glasgow G12 8QQ, United Kingdom
(2) Institute of Aquaculture, University of Stirling, FK9 4LA, Stirling, United Kingdom
(3) Aquaculture Innovation, 1/1 34 Lawrence St, Glasgow G11 5HP, United Kingdom
*Corresponding author: [email protected]
Summary
As currently practised, the culture of fish for food potentially raises concerns
about the welfare of farmed fish, and this is a topic that has received considerable
attention. As vertebrates, fish share a number of features with the birds and
mammals that are more commonly farmed, so many welfare principles derived
from consideration of these groups may also be applied to fish. However, fish
have a long, separate evolutionary history and are also adapted to a very different,
aquatic environment. For these reasons, they have a number of special features
that are relevant to how welfare is defined, assessed and promoted and these are
discussed. The various methods that are available to researchers for identifying
and assessing good and bad welfare in fish are considered, including assessment
of physical health and physiological, behavioural and genomic status. The subset
of practical welfare indicators that can be used on working farms is also reviewed.
Various aspects of intensive aquaculture that can potentially compromise fish
welfare are outlined, as are some strategies available for mitigating such adverse
effects. Finally, the paper ends by looking briefly to the future, identifying likely
changes in aquaculture practices and how these might affect the welfare of
farmed fish.
Keywords
Aquaculture – Behaviour – Feelings – Function – Health – Naturalness – Stress physiology
– Welfare.
Introduction
Whatever the purpose for which finfish (hereafter simply
referred to as fish) are cultured, whether for the aquarium
trade, scientific research or restocking (1), it is important
to ensure the well-being of the fish concerned. The culture
of fish for human consumption, i.e. fish farming, currently
provides more than 50% of the fish we eat, is growing
rapidly (approximately 9% per annum for the past three
decades), and is becoming more intensive (2). The welfare
of such fish, particularly those reared intensively, forms the
topic of this review.
Being vertebrates, fish have many traits in common with the
more familiar intensively farmed animals such as pigs and
chickens. However, as an ancient group of vertebrates, and
being aquatic, they differ from terrestrial animals in ways
that are important when it comes to welfare. The authors
therefore begin this paper with a brief account of the special
features of fish, and then consider the challenging issues
of what welfare means and the extent to which the term
can appropriately be applied to fish. The authors conclude
cautiously that the term can be meaningfully applied and
so they then discuss how good and bad welfare can be
identified and assessed, both during scientific research
and on working fish farms. They then consider the ways
in which intensive fish culture can potentially compromise
fish welfare and the kinds of actions that have been and
could be taken to promote the welfare of farmed fish now
and in the future.
234
An important point to make first is that the taxonomic group
Pisces has been in existence for some 500 million years,
compared to 150 and 200 million for birds and mammals,
respectively, and comprises about 28,500 living species, all
adapted for coping with the challenge of their particular
ways of life. For this reason, when it comes to defining,
assessing and protecting fish welfare, it is important to
avoid projecting what we know of birds and mammals
onto fish or assuming that fish are in some way inferior to
terrestrial animals. On the contrary, arguably their longer
phylogenetic history makes them a particularly successful
group. Furthermore, although the various kinds of fish have
many things in common, they are phylogenetically and
ecologically diverse. Legitimate generalisations can be made
about fish welfare, but specific details of what promotes or
detracts from good welfare will vary from species to species.
What is special about fish?
Almost all fish share a similar basic body plan with other
vertebrate groups, having among many other traits an
anterior, jawed skull, a spinal column and two sets of paired
appendages (fins in the case of fish), all made of bone or
cartilage. Also, the structure and function of the nervous
system are broadly similar, with a central nervous system,
consisting of a brain and spinal cord, connected to the sense
organs and the muscles by a peripheral nervous system.
Overall, the sense organs of fish are remarkably similar in
structure and function to those of terrestrial vertebrates, as
is the endocrine system, including the hormones involved
in stress responses (3). Fish are also similar to other
vertebrates in terms of their general behavioural capacities:
they show the same kinds of learning and navigate around
their environment using similar cognitive processes. Like
other vertebrates, they have behavioural traits that enable
them to find, capture and ingest appropriate food, to avoid
becoming food themselves and, depending on the species,
to fight, court and mate and, in some cases, to take care of
their young (1).
On the other hand, having had a separate and longer
evolutionary history than birds and mammals, and being
adapted to live permanently in water, fish differ from other
vertebrate groups. Some of the differences that are most
relevant to the question of fish welfare are outlined in
Table I. Arguably, the relatively small size and simplicity of
the brain and the very different way in which it develops
are particularly important, as they could mean that fish lack
the behavioural and cognitive complexity needed for the
concept of fish welfare to be meaningful. An additional and
significant practical consequence of the aquatic habitat in
which fish live is the fact that it can be difficult for humans
(scientists or farmers) to gain access to them for the purpose
of monitoring welfare.
Rev. sci. tech. Off. int. Epiz., 33 (1)
What does welfare mean and
does the concept apply to fish?
The second section of this volume discusses the question
of what welfare means when applied to animals in general.
The authors revisit the topic here because much of the
controversy concerning fish welfare arises from the different
ways in which animal welfare can be defined. Briefly, some
would propose that an animal experiences good welfare if it
can adapt to its environment and is in good health, with all
its biological systems functioning appropriately. According
to this function-based view, an animal that is in poor health
has poor welfare by definition, and vice versa. Another view
proposes that to enjoy good welfare an animal must be
able to lead a natural life, such that, by definition, welfare
is compromised if a captive animal cannot show the full
repertoire of behaviour that it would display in the wild. A
third position equates good welfare with an animal being
largely free from negative feelings, such as pain, fear and
hunger, and having access to positive experiences, such as
companionship for social animals. None of these positions
is right or wrong; they simply emphasise different aspects
of a complex phenomenon (4). Table II explores some
implications of these different approaches to welfare with
respect to two situations that farmed fish may experience;
namely, poor body condition related to low nutrient intakes
and involvement in fights.
The thought that an animal may be suffering is a strong
driver for concern about animal welfare, so definitions
based on feelings probably best address public sentiment
on this matter. It is therefore important that scientists
address this aspect of welfare. The question of whether
fish have the capacity for suffering, which in turn depends
on just how complex their cognitive and emotional
capabilities are, continues to be hotly debated. The answer
is important, since it will determine whether the concept
of welfare defined in terms of feelings is applicable to fish,
an issue that is considered in detail by Braithwaite and
Ebbesson (7).
Briefly, the view that fish do not have the capacity for suffering,
clearly articulated by Rose (8, 9, 10), is based on, among
other things, the fact that the fish brain is small compared to
that of mammals and lacks structures that underpin many
higher mental processes in humans. In addition, according
to this view, fish have little capacity for learning and a short
memory span. While they have the mechanisms to detect
and respond to harmful stimuli and potentially dangerous
events, such responses, though perhaps more than simple
reflexes and possibly with some emotional content (10), are
thought to fall far short of what could be called feelings.
However, others have argued against this view (e.g. 11, 12,
13), partly because the behaviour of fish is more complex
235
Rev. sci. tech. Off. int. Epiz., 33 (1)
Table I
Some differences between fish and other vertebrates and the environments in which they live, together with potential implications for
the welfare of farmed fish (1, 3)
Special features of fish and their environment
Some implications for fish welfare
Water
–
Water is a dense medium, so fish are constrained by hydrodynamic
demands and fast swimming can be costly
–
In addition to their streamlined shape, fish secrete a layer of mucus over
their skin that lubricates their movement and provides protection from
external infection; the integrity of this layer is important for health
–
Gases dissolve readily in water, but moving water for oxygen
extraction is energetically costly
–
Extracting oxygen from and secreting carbon dioxide into water is relatively
easy
–
Many other chemicals readily dissolve and disperse in water
–
Water can potentially carry many harmful substances
Respiration
–
The respiratory tissues of fish (the gills) have a large surface area
in direct contact with water for gas exchange
–
Many ions pass readily between fish and water through the gills, making
osmoregulation challenging
–
Unlike air-breathing animals, the respiratory tissues of fish do not
show an in situ immune response
–
Fish are particularly vulnerable to harmful chemicals in the water and fish
can be exposed to a greater pathogen load via respiration
–
For proper functioning, fish are dependent on exposure to an appropriate
range of environmental temperatures. Access to a thermal gradient within
the environment allows fish to greatly increase the efficacy of their innate
immune response. At low temperatures the energetic needs of fish are
reduced and periods without food are neither unnatural nor necessarily
deleterious
–
Each life-history stage has specific conditions that optimise welfare
–
Fish have an additional line of defence against pathogens that has not yet
been incorporated into disease prevention or treatment systems
Temperature
–
Fish are ectotherms, meaning that they do not maintain a constant
temperature physiologically; fish body temperature follows water
temperature, which can be adjusted behaviourally by tracking water
of particular temperatures
Life history
–
Many species of fish undergo, to a greater or lesser extent, dramatic
changes in form and function between life-history stages
Immunity
–
Unlike mammals, but in common with birds, fish red blood cells are
nucleated, giving them additional functions including immune responses
Sensory environment
–
The sensory environment in water is different from that in air; e.g. light
attenuates quickly in water and wave length changes with depth
–
The right photic conditions are needed for visually feeding fish to detect
food; e.g. zooplanktivores need ultraviolet light to capture food efficiently
–
Mechano-sensory cues travel well in water and fish are very sensitive to
vibration through the lateral line system
–
Fish behaviour may be disrupted by ambient sound
–
Many fish are able to detect and produce electric fields and use this for
orientation and communication
–
Background electrical fields may disrupt behaviour in such cases
Fish density
–
Many species of fish live in large, coordinated social groups or schools
–
Relatively high fish densities may not be detrimental
–
Intensive fish farming is relatively new. Strains of a few species have been
reared in captivity for several generations, but the process of domestication
is much less advanced than for birds and mammals
–
There has been less time for welfare-friendly traits such as lack of fear or
low levels of stress responsiveness to develop
than commonly recognised and also because there is a fair
degree of homology and functional equivalence between
the brains of fish and mammals. In particular, two parts of
the forebrain involved in the generation of emotions and in
learning in mammals, i.e. the amygdala and hippocampus,
respectively, have anatomical and functional homologues in
the brains of fish. Clearly, we need to know a great deal
more about the mental and emotional life of fish before this
issue can be resolved, but the authors conclude that fish
have some degree of consciousness or sentience, no doubt
different in kind and intensity from that of humans. In
the specific context of assessing the well-being of cultured
fish, the question is somewhat academic, since most of the
ways that scientists can use to assess the welfare of fish held
under production conditions relate to functioning rather
than feeling.
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Rev. sci. tech. Off. int. Epiz., 33 (1)
Table II
Some implications of defining animal welfare in terms of proper biological functioning, what is natural and what fish feel, illustrated
with reference to fish in a poor state of nutrition and taking part in fights (1, 5, 6)
Type of definition
Implications of each kind of definition
Poor nutritional status
Fighting and aggression
Functional
Are the fish
in poor health?
Whether loss of appetite and depleted energy reserves
should be interpreted as poor welfare depends on
circumstance and on individual status. For example,
failure to feed may be a sign of poor welfare in a juvenile
Atlantic salmon in the summer, but not necessarily in the
winter, when a subset of each cohort undergoes a period
of adaptive natural anorexia. Their physiological processes
are adjusted accordingly and thin fish are functioning just
as they ought to be
Wild male salmon fighting to gain access to spawning females
after having swum hundreds of miles up-river without feeding have
markedly depleted energy reserves, may well be injured and are likely
to have impaired immune function. However, these are costs incurred
in the interest of gaining the fitness benefits of breeding opportunities.
Natural physiological processes allow mature fish to fight and
breed effectively and subsequent thinness and injury are normal
consequences of these
Natural
Can the fish engage in
natural behaviour?
Since millions of wild fish fail to gain enough food, poor
nutritional status and death from starvation occur in
the wild. On a strict interpretation of a nature-based
definition, these do not in themselves indicate poor
welfare
Fighting is a natural behaviour in very many species of fish. Any
resulting stress or injury, or the failure of losers to get food or mates,
does not necessarily reflect poor welfare. Arguably, denying fish the
opportunity to fight may impair their welfare
Feelings-based
Are the fish free from
negative feelings?
If fish are sentient, then how thin fish feel about poor
nutritional status dictates whether their welfare is good
or bad. Fish with low energy reserves may not feel bad
if they are not motivated to feed. In juvenile Atlantic
salmon displaying winter anorexia, the energy reserve
threshold at which they become motivated to feed is
reset downwards; a level of reserves that would generate
appetite in summer does not do so in winter
Whether an animal that is stressed or injured as a result of fighting
experiences poor welfare depends on whether these states generate
negative feelings and emotions. The fitness consequences of winning
a fight may be so high that, when in an appropriate physiological state,
fish may be highly motivated to take part in contests. Again, it may
be that denying fish the opportunity to do so may compromise their
welfare
Assessing the welfare
of farmed fish
Assuming that the welfare of farmed fish matters, to
determine if it is compromised by aquacultural practices
and to monitor the effectiveness of attempts to improve
it, accurate and objective ways of assessing fish welfare
status are needed. Our knowledge of the effects on fish of
the natural challenges they experience in the wild suggests
that there are a number of approaches to this task. These
approaches, most of which address welfare in terms of
function rather than feelings, are listed with examples in
Table III. Starting with what is perhaps the most obvious,
good health is recognised as critical for fish welfare and
signs of injury or infection are important indicators of poor
welfare (19). So too is the status of the immune system,
which reflects a fish’s ability to fight off disease (20).
It can be hard to interpret just what good or poor health
indicates about welfare. Many would consider that an
unhealthy fish is in a poor state of welfare by definition, as
a direct result of the disease. However, the converse may
not be true, as a fish that is healthy may still experience
poor welfare, for example if held in an inappropriate social
environment. Because stress can suppress immune function
and so increase the risk of infection, a high incidence
of disease and mortality can point towards underlying
problems with the fish’s environment, although even fish
experiencing optimal conditions may suffer from disease
and serious epidemics do occur in populations of wild fish.
Physical variables such as level of nutritional reserves,
rates of growth and reproductive status also provide
information on the welfare of the fish concerned, because
various challenges interfere with feeding, which in turn
can compromise growth and reproductive development.
Reduced appetite is one of a number of short-term changes
induced by activation of a physiological stress response,
which includes the release of the hormones adrenaline
and cortisol from the inter-renal glands. Adrenaline is not
an easy hormone to measure because it is released rapidly
in response to handling stress, but indirect indicators
of adrenaline release can be used, including faster gill
ventilation and increased oxygen consumption or heart
rate. Cortisol is easier to measure because handling-
237
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Table III
Measures of fish welfare used by aquaculture researchers in studies of the effects of stocking density
Measure
Example of use in aquaculture research
Health status
Injury
–
–
In rainbow trout reared at different stocking densities, anal fin condition was better at lower densities, whereas dorsal fin
condition was better at higher densities (14)
Number of skin lesions decreased with stocking density in African catfish (Clarias gariepinus) (15)
Disease status
–
–
Ayu held at high densities showed higher levels of mortality, probably due to bacterial infection (16)
Disease outbreaks were common in Senegalese sole held at high stocking densities (17)
Immune responses
–
Ayu held at high densities showed suppressed serum immunoglobulin M levels (16)
–
There was an inverse linear relationship between stocking density and plasma amino acid concentrations (reflecting recent
Physical status
Nutritional status/physiology
metabolic history) in Senegalese sole, perhaps due to increased stress levels (17)
Growth
–
In rainbow trout reared at different stocking densities, growth rates and feed utilisation efficiency were reduced at higher
densities (14)
Respiratory activity
–
Air breathing increased with stocking density in African catfish (15)
Stress hormones
–
–
Ayu held at high densities showed elevated plasma cortisol concentrations (16)
Senegalese sole held at high densities had high plasma cortisol concentrations (17)
Food intake
–
Individual daily feed intake was reduced in African catfish of ca 200 g held at a low stocking density (15)
Swimming
–
Swimming activity was lower in African catfish held at low stocking density (15)
Stereotypical behaviour
–
African catfish held in high-density groups show stereotypic behaviour in the form of continuous circling in a small area of the
holding tank, especially during the night when these fish are normally active (18)
Physiological status
Behavioural status
induced increases are relatively slow, and elevated plasma
cortisol levels thus feature prominently as an indicator of
possibly impaired welfare. The relationship between such
short-term responses to stress and fish welfare is complex,
because they are part of a natural and adaptive response to
challenge (21). There is no particular reason to suggest that
the temporary physiological activation that prepares fish
for activity is detrimental to welfare and in some contexts
such short-term responses may be beneficial. Even so, most
would agree that evidence of chronic, unavoidable stress in
farmed fish indicates compromised welfare, so although a
focus on stress does not fully capture the complexities of
animal welfare, monitoring stress responses may give us an
important part of the picture.
Since altered behaviour is an early and easily observed
response to adverse conditions, monitoring behaviour is
important in assessing fish welfare (22). Potential behavioural
indicators of poor welfare include loss of appetite, natural
signs of distress such as erratic swimming and performance
of persistently repeated actions, or stereotypies. An
approach that may provide a better understanding of what
fish feel focuses on learned responses. For example, fish
such as Atlantic salmon and Atlantic cod can be trained to
associate a flashing light in one location with the imminent
presentation of food somewhere else, even when there is a
delay between the end of the light signal and the appearance
of food. Trained fish move into the area where they have
come to expect food after the light has stopped flashing
but before the food has arrived, showing anticipation of
the reward. The anticipation response disappears when fish
are stressed and this turns out to be a particularly sensitive
indicator of stress. Using computer-aided image analysis,
such responses can be quantified, even in fish held at high
densities, so they have the potential to provide a sensitive
non-invasive indicator of welfare in intensively farmed
fish (23).
Since the array of methods for assessing fish welfare all
reflect something slightly different, we need some way to
combine them into an integrated picture of welfare status
as a whole. One approach is to use statistical analysis of
relationships among the various measures to combine these
into an overall welfare score. For example, Turnbull et al.
238
(24) used multivariate analysis to combine four separate
measures of welfare in Atlantic salmon held at different
stocking densities. This generated a single welfare index
to which fin condition and nutritional status contributed
positively and plasma cortisol and glucose negatively. This
score was highest, in other words the overall welfare of the
fish was best, at an intermediate density of 25 kg as opposed
to 15 kg or 35 kg per m3.
A very different approach to gaining a broad oversight of the
welfare of farmed fish is potentially provided by using modern
molecular tools to explore patterns of gene expression in fish
exposed to different challenges (25). Information obtained
from studying the complete set of RNAs encoded by the
genome of (in this case) a fish held under a specific set of
conditions (genome-wide transcriptomics), complemented
by the huge amount of information on the functions of
known genes in other organisms, can give an integrated
picture of the overall response of fish to aquaculture-related
challenges. For example, in seabass, discrete clusters of
genes can be identified based on their specific temporal
patterns of expression following confinement stress.
These patterns of expression are related to rapid metabolic
activation, tissue repair and remodelling, reestablishment of
cellular homeostasis and immune regulation (26).
Also of interest is the expression of candidate genes
whose effects are known and can confirm and extend
understanding of the effects of key stressors. For example,
short-term crowding in Atlantic cod is associated with
up-regulation of genes involved with glucose transport
and with inflammatory and antibacterial responses (27),
reflecting the complex adaptive response to the challenge
of high densities. The responses of candidate genes can also
identify potential early warning signs of stress. For example,
in young seabass acute confinement stress strikingly
increases the ratio between a precursor of brain-derived
neurotrophic factor (pro-BDNF) and mature BDNF, which
potentially provides a reliable biomarker that could be used
to detect stress in seabass (28).
Rev. sci. tech. Off. int. Epiz., 33 (1)
expensive and often require fish to be handled while
samples are collected. In contrast, monitoring the welfare
status of cultured fish requires systems that are effective,
economical and practical for use under farming conditions.
A range of non-invasive, relatively simple, but accurate
ways of monitoring fish welfare on working farms, i.e.
operational welfare indicators, are available. These include
routinely gathered production indicators such as mortality,
fish health, feed conversion efficiency and growth rates, as
well as osmoregulatory status at critical periods, such as the
transition from fresh to salt water (smolting) in salmonids.
Depending on circumstances, other indicators that are
observed or monitored by fish farmers include fin and body
condition, body coloration (which may reflect stress levels),
feed intake, ventilation rate and patterns of swimming. In
this context, it is worth emphasising that good fish farmers
know how to assess the well-being of their stock and have
much of value to teach scientists (24).
A different, indirect approach to estimating the welfare
of farmed fish, based on what is known about the effects
of physical and social conditions on their well-being, is
to measure not the fish themselves but the environment
in which they are farmed. Water quality is particularly
important in this context, and commonly measured
variables include temperature and dissolved oxygen. More
recently, dissolved carbon dioxide has been included, as
elevated levels may not only cause discomfort, but may also
indicate that stock are stressed and hyperventilating. Other
variables that are monitored where appropriate include pH
levels and the presence of heavy metals in the water.
Promoting
the welfare of farmed fish
Looking, in fish, for candidate genes known to be related
to cognitive and emotional states in mammals offers an
additional tool for addressing the difficult question of
sentience in fish. As an example, comparison of candidate
genes for corticoid receptors in the brains of different
strains of rainbow trout (i.e. those selected for high
stress responsiveness and those selected for low stress
responsiveness) suggests that site-specific differences in
mineralocorticoid receptor expression may be responsible
for strain differences in memory and in appraisal of negative
stimuli, both of which are cognitive traits that are related to
sentience (29).
A number of aquaculture practices can potentially
compromise the welfare of farmed fish. The most important
of these practices are summarised in Table IV. Welfare
scientists, veterinarians and the aquaculture industry have
worked together to develop a number of ways of mitigating
the effects of these practices. One strategy is to make a
careful choice of which fish to culture, since some species
and strains of fish are less easily stressed and therefore more
amenable to being held in captivity than others. Arguably,
these are the species and strains that should be used in
food aquaculture. Such suitable forms may be natural
variants. For example, in many high-latitude lakes different
forms of Arctic charr coexist, feeding selectively on either
zooplankton or large, benthic invertebrates. The planktonfeeding form is less aggressive than the benthic-feeding
form (31) and arguably more suitable for culture.
Many methods used by researchers for measuring fish
welfare are time consuming, technically demanding,
Alternatively, suitable fish for intensive culture may be the
result of a degree of domestication or targeted selection. In
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Table IV
Some possible adverse effects of husbandry practices
on the welfare of farmed fish (30)
Husbandry
practice
Possible adverse effects
Feeding
Failure to provide an appropriate diet in an
attractive form may result in malnutrition
Failure to provide the right amount of food at the
right time may mean that fish do not feed well
Failure to make food accessible to all fish in a
cage/tank may mean that some fish experience
malnutrition
Stocking density
Stocking densities that are either too high or
too low can have negative effects on welfare,
depending on species and life-history stage,
through interacting effects of water quality and
aggression
Disease and
disease treatment
Farmed fish are more vulnerable to disease than
their wild counterparts, but disease treatments
and vaccinations may themselves cause damage
and stress to fish
Grading
Fish are graded to produce like-sized groups for
efficient husbandry and potentially to prevent
attacks by much larger fish, but grading and the
handling this involves can itself cause damage
and stress
Transport
Transport often involves handling, crowding,
vibration, poor water quality and other adverse
environmental conditions
Slaughter
Slaughter often involves handling, crowding,
exposure to alarm cues and, for some methods,
pain
species such as brown trout and Atlantic salmon, which have
been farmed intensively for a number of generations, fish
from cultured strains often show weaker behavioural and
physiological responses to disturbance than do their wild
counterparts (1, 32). When kept in mixed groups, rainbow
trout selected for low stress responsiveness grow faster than
companions selected for high stress responsiveness (33).
Feed waste is higher and feed conversion efficiency lower
in fish with a high stress response (34).
Within species and strains, there is variation in how
individual fish respond to novelty and risk, often linked to
differences in stress physiology (35). Where domesticated
strains are not available, one possible approach might
be to identify and screen out risk-averse fish early in the
production cycle. Age of first feeding is a possible selection
criterion, since, in salmonids at least, this predicts responses
to a potential risk in later life, e.g. the rate at which fish start
feeding after being isolated (36).
A different, complementary approach is to develop
husbandry practices and management systems that
minimise threats to welfare. In traditional, extensive
aquaculture, such systems have been in place for many
years and in intensive aquaculture much effort has recently
been devoted to this issue. For example, there has been an
increase in the use of strippers to reduce carbon dioxide
levels in tanks and in the development and deployment
of land-based recirculation systems in which the water is
continually treated to ensure optimal conditions for fish
(37). At a different level, strategically placed underwater
lights can be used to encourage fish to use more of the
available space, thereby reducing crowding (38). Using
interactive feeders that deliver food whenever fish are
hungry rather than at pre-defined, predictable times
of day creates a farm environment in which there is less
competition for food, and fish that are poor competitors
are able to feed and grow well (39, 40). Another method of
minimising threats to welfare is to incorporate into fish feed
a precursor of serotonin, which is produced naturally in the
central nervous system, as this reduces levels of aggression
in several species of farmed fish (41). Also, Lines and
Spence (42) give examples of the development of methods
of humane slaughter for fish (see also 43).
Alternatively, for each species and life-history stage,
simple, but accurate, indicators of welfare can be used
on working farms as ‘early warning systems’ for emerging
welfare problems. The known short- and medium-term
responses of fish to adverse conditions point to a number
of indices that could potentially be monitored in fish in
production conditions without any need for disturbing
them, except perhaps by placing cameras in cages. Some
of these have been discussed above, including changes in
colour, ventilation rate and patterns of swimming, as well
as reduced food intake, loss of body condition, damaged
fins and slow growth. Recent studies have highlighted the
possibility of using computer-based video analysis of the
movement patterns of fish in working production cages to
pick up changes that might indicate poor welfare (e.g. 44).
Thus, there are many ways in which the welfare of farmed
fish can potentially be promoted, but it is important to know
what the full economic consequences are likely to be. This is
not simple, since it requires detailed information about the
impact of the intervention upon all aspects of production,
on the costs of the whole production chain and, given the
possibility of a welfare premium in the marketplace, on the
attitudes and behaviour of consumers. Bioeconomic models
have been developed that integrate these different strands
and predict the impact of any given welfare intervention on
profitability across the production chain (45). For example,
such modelling reveals that carbon dioxide stripping in
Atlantic salmon smolt production would increase both
profits and welfare, whereas, in the case of demand feeders,
improved fish welfare comes at an economic cost. Such
240
models provide the aquaculture industry and regulatory
bodies with the information needed to incorporate
appropriate welfare interventions into modern, sustainable
aquaculture.
The welfare of farmed
fish in the future
There is little doubt that fish farming will continue and most
likely expand in the future and several aspects of the way
in which fish are farmed are likely to change, with possible
implications for welfare (46, 47). A wider range of species
is likely to be cultured, and the farming conditions that
optimise welfare will need to be established for each new
species and life-history stage. Depending on the location
and the species concerned, production systems may well
become more intensive. At one extreme these intensive
systems may take the form of very large offshore cages and,
at the other extreme, small units supplying fish locally.
Meeting biological needs, stock monitoring and
environmental control are all increasingly challenging
technologically in larger, more intensive systems, while
being economically challenging in smaller-scale intensive
units. Effective use of such systems will depend on
technological advances, including increased use of landbased recirculation systems. Water quality can be a challenge
in recirculation systems, which can be optimised if designed
properly. However, a heavy reliance on technology renders
back-up systems essential, as poor welfare is implicit in the
event of technological failure.
Intensive fish farming will almost inevitably lead to the
development of new diseases with associated welfare
impairment unless suitable forms of treatment, prevention
or management are developed. In intensive fish farming,
veterinary care has for many years focused upon disease
management, i.e. what might be called ‘firefighting’. In
spite of improved vaccines and other treatments and
modern diagnostic tools, overall mortalities on fish farms
have not been reduced in the past two decades (salmon:
Kontali Analyse, unpublished data; seabass and seabream:
N. Steiropoulos, personal communication). Furthermore,
few veterinary courses include more than a passing reference
Rev. sci. tech. Off. int. Epiz., 33 (1)
to fish and aquaculture. As aquaculture grows rapidly, there
will be an increased need for veterinary graduates who have
an interest in and capacity to care for large fish populations.
It is also important that the industry moves towards a
paradigm of preventative fish health management, with
veterinarians participating as members of fish production
teams that seek to minimise losses due to disease by
monitoring husbandry practices, water quality, equipment,
biosecurity and other factors pertinent to fish welfare.
One way of ensuring good welfare and good production
in increasingly intensive fish culture is to use selective
breeding programmes to generate fish that flourish in such
systems. The authors predict that, in the future, this is likely
to be informed by molecular technologies (see above),
which can, for example, identify biomarkers for favourable
fish from an early age, streamlining and speeding up the
selection process.
In terms of public relations, on the one hand there is likely
to be increasing public concern about the welfare of farmed
fish and the environmental impacts of aquaculture systems,
a concern that may potentially be mitigated by helpful
explanations provided both by farmers and researchers.
On the other hand, there are early indications of beneficial
changes in public attitudes, with a growing recognition
that aquaculture can contribute to the provision of healthy
food without depleting natural fish stocks. There is also
increasing global investment in fish farming, a change that
is likely to result in farmed fish being regarded even more
as commodities than at present, pointing to an even greater
need to ensure that their welfare is protected.
Acknowledgements
The authors would like to thank Simon MacKenzie and
Alan Dykes for discussions of the issues considered in this
article and a referee for helpful comments on an earlier
version of this chapter.
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Rev. sci. tech. Off. int. Epiz., 33 (1)
Définir, évaluer et promouvoir le bien-être des poissons d’élevage
F.A. Huntingford & S. Kadri
Résumé
Telle qu’elle est pratiquée actuellement, l’aquaculture destinée à fournir la filière
agroalimentaire présente des aspects potentiellement préoccupants quant au
bien-être des poissons élevés dans ce contexte ; cette question fait désormais
l’objet d’une grande attention. En tant que vertébrés, les poissons ont plusieurs
caractéristiques communes avec les principales espèces d’oiseaux et de
mammifères élevées par l’homme, de sorte que nombre de principes de bien-être
animal pertinents pour ces groupes d’animaux sont également valables pour les
poissons. Néanmoins, en plus d’avoir une histoire évolutive longue et distincte,
les poissons ont aussi dû s’adapter à un environnement aquatique, par nature très
différent. Pour toutes ces raisons, les poissons possèdent en propre certaines
caractéristiques particulières qui jouent sur la manière de définir, d’évaluer et
de promouvoir leur bien-être. Les auteurs examinent ces aspects, ainsi que les
méthodes dont disposent les chercheurs pour identifier et évaluer les bonnes ou
mauvaises conditions de bien-être chez les poissons, en particulier pour évaluer
leur état de santé physiologique et psychologique, leur comportement et leur
statut génomique. Ils décrivent également une série d’indicateurs concrets du
bien-être qui peuvent être utilisés dans les élevages. Ils soulignent les divers
aspects de l’aquaculture intensive qui risquent de compromettre le bien-être des
poissons et présentent quelques stratégies pour atténuer ces effets négatifs.
Enfin, ils font rapidement le point sur les perspectives d’avenir en exposant
l’évolution probable des pratiques en aquaculture et leurs conséquences sur le
bien-être des poissons d’élevage.
Mots-clés
Aquaculture – Bien-être animal – Comportement – Émotions – Expression naturelle –
Fonction – Santé – Stress physiologique.
Definición, evaluación y fomento
del bienestar de los peces de cultivo
F.A. Huntingford & S. Kadri
Resumen
La piscicultura con fines alimentarios, tal como se practica actualmente, puede
generar problemas ligados al bienestar de los peces de cultivo, y este es un
tema que ha merecido considerable atención. Los peces, como vertebrados
que son, comparten diversos rasgos con las aves y mamíferos que más
frecuentemente viven en granjas, por lo que también cabe aplicar a los peces
numerosos principios de bienestar pensados para dichos grupos. Sin embargo,
los peces tienen una historia evolutiva larga e independiente y además están
adaptados a un medio muy distinto, el acuático. Por ello presentan una serie
de características especiales que entran en juego a la hora de definir, evaluar
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Rev. sci. tech. Off. int. Epiz., 33 (1)
y fomentar su bienestar, características que los autores enumeran y examinan.
También exponen los diversos métodos de que disponen los investigadores
para reconocer y determinar en los peces estados positivos y negativos de
bienestar, lo que incluye la evaluación de su salud física y su estado fisiológico,
comportamental y genómico. Asimismo, pasan revista al subconjunto de
indicadores prácticos de bienestar que pueden utilizarse en las piscifactorías, y
destacan varios aspectos de la acuicultura intensiva que pueden comprometer
el bienestar de los peces, así como una serie de estrategias disponibles para
mitigar esos efectos adversos. Para concluir, se refieren brevemente al futuro,
señalando la evolución que presumiblemente seguirá la praxis de la acuicultura
y la forma en que estos cambios podrían repercutir en el bienestar de los peces
de cultivo.
Palabras clave
Acuicultura – Bienestar – Comportamiento – Emociones – Fisiología del estrés – Función
– Naturalidad – Salud.
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