3. Domestication and welfare

#### 3.1. Genes

In the artificial conditions provided by human farming activities, it is likely that the most successful phenotypes of farmed animals are different from those under natural conditions. However, that does not mean that these selected phenotypes carry differential genotypes, especially due to phenotypic plasticity which is remarkably relevant in fish: different populations of the same species present contrasting yet plastic behavioural responses to environmental and social conditions [32–38]. Nevertheless, artificial selection experiments demonstrate that almost any quantitative trait could be permanently altered, that responses (mostly) occurred as a consequence of changes in the frequencies of genes affecting the traits, and not from mutations, and that many genes must be involved [39, 40].

effects. Conversely, the low number of generations in the rapidly increasing, diverse and generally very recent fish farming activity may be too short to permit this adaption in aquatic

Domestication and Welfare in Farmed Fish http://dx.doi.org/10.5772/intechopen.77251 115

Changes in the phenotypes of selected farmed fish usually correlate with changes in physiological indicators. For example, when comparing seventh-generation farmed Atlantic salmon with wild individuals, the domesticated fish grow much faster (even more so in salt water where the difference is threefold), pituitary and plasma growth hormone levels were positively correlated with growth rate and significantly higher in the domesticated strain [45]. The same occurs with strains of Brook trout (Salvelinus fontinalis) farmed for 30 or more years (ca. 10 generations). The domesticated phenotype is less resilient than the wild, since hatchery-born fingerlings struggle to survive when released into native streams. Moreover, domesticated strains grow better in aquaculture but not in the wild [46], which led some authors to claim that domesticated animals are better adapted to captivity, reducing stress and mortality, increase disease resistance, reduce the use of chemotherapeutics and contribute to better animal welfare and environmental management. Up to 65% of farmed salmon in Norway comes from improved breeding plans, after an extensive programme lasting over 40 years and an enormous investment effort, with numbers reaching nine digits [26]. However, and despite these efforts and claims, 40 years represent only 10–13 generations of farmed salmon (Figure 1). Even more importantly, a recent analysis of welfare conditions of farmed salmon revealed a need for improvement in space, substrate, aggression, stress levels and malformations ([47], see Salmo salar). A possible conclusion is that the improvement programme of salmon in Norway may be focusing mostly on production-related traits. Although there are improvements on the health perspective of welfare, the natural needs

and behaviour of this species in captivity may be generally impaired.

For many physiological indicators such as those listed below, selected strains of farmed fish fail

Metabolic rate: fast growing hatchery strains of Rainbow trout present higher standard metabolic rate (SMR), lower aerobic scope, and potentially lower maximum metabolic rates, suggesting that high growth trades off against a reduced capacity to do metabolic work. Higher SMR of fast growers appears to be related to a greater investment in high-maintenance digestive tissue that supports rapid growth, which appears to compromise active metabolism [48]. Farmed Senegalese sole (Solea senegalensis) born from wild spawners are nevertheless capable of shifting their routine metabolism from naturally nocturnal to diurnal, responding

Hypoxia resistance: triploid strains of domesticated Rainbow trout show faster growth than wild diploid individuals probably due to impaired gametogenesis of 3n fish [50]. Adding to these reproductive problems, triploids are also less resistant to hypoxia [51], which can account for lesser resistance and higher mortalities both in nature [52, 53] and in several types

species.

3.2. Physiology

to show positive results:

to daylight feeding regimes [49].

of farming conditions and methods [54–57].

In livestock species, genetic selection has greatly increased production levels. Usually, the breeding goal is to create a population with high economic production efficiency, i.e. high production combined with relatively low feed intake. Breeding programs have become quite successful because of the high accuracy of breeding value estimation, the moderate to high heritabilities of most production traits and the use of large and fast databases containing production records of many animals and their genetic relationships. Apart from genetic changes, production is also increased by improvement of housing, feed composition, feeding strategies, health status and farm management.

However, negative side-effects of domestication largely occur and are expected to increase when the focus continues to be only on production efficiency. Animals in a population that has been genetically selected for high production efficiency seem to be more at risk for behavioural, physiological, immunological, reproductive and consequently welfare problems [41]. This occurs because behavioural traits, as well as the other typical components of the domestication phenotype (growth, stress, immune function, etc.), are most likely controlled by many genes, i.e. they are polygenic [15]. In addition, a given set of genes may influence different traits, a mechanism known as pleiotropy [42]. In such a case, increasing the frequency of alleles that, for example, up-regulate growth, may at the same time modify other essential welfare-related traits under the influence of the same genes. Finally, the function of one gene may also be influenced by the interaction with other genes, which is known as epistasis [43]. Selection for one or a few traits controlled by genes that have epistatic effects may thus influence a group of other genes, regulating other characters than those selected for. Therefore, both mechanisms (pleiotropy and epistasis) are more than likely to create side-effects on traits that are not desirable [15]. In fact, when animals are selected for production traits mainly, many side-effects have been extensively documented in several species [41]. Some of these side-effects will even affect production itself, such as reduced fertility in fast- growing broilers [41], and are likely to be the target of counter-selection. In other cases, the side-effects may be related to less-obvious traits which may nevertheless have a strong welfare aspect [44] because they shift welfare optima towards unknown directions. These processes have occurred in land animals throughout their domestication. However, the slow and long domestication process on land has allowed both humans and many livestock species to adapt and cope with such effects. Conversely, the low number of generations in the rapidly increasing, diverse and generally very recent fish farming activity may be too short to permit this adaption in aquatic species.

#### 3.2. Physiology

3. Domestication and welfare

In the artificial conditions provided by human farming activities, it is likely that the most successful phenotypes of farmed animals are different from those under natural conditions. However, that does not mean that these selected phenotypes carry differential genotypes, especially due to phenotypic plasticity which is remarkably relevant in fish: different populations of the same species present contrasting yet plastic behavioural responses to environmental and social conditions [32–38]. Nevertheless, artificial selection experiments demonstrate that almost any quantitative trait could be permanently altered, that responses (mostly) occurred as a consequence of changes in the frequencies of genes affecting the traits, and not

In livestock species, genetic selection has greatly increased production levels. Usually, the breeding goal is to create a population with high economic production efficiency, i.e. high production combined with relatively low feed intake. Breeding programs have become quite successful because of the high accuracy of breeding value estimation, the moderate to high heritabilities of most production traits and the use of large and fast databases containing production records of many animals and their genetic relationships. Apart from genetic changes, production is also increased by improvement of housing, feed composition, feeding

However, negative side-effects of domestication largely occur and are expected to increase when the focus continues to be only on production efficiency. Animals in a population that has been genetically selected for high production efficiency seem to be more at risk for behavioural, physiological, immunological, reproductive and consequently welfare problems [41]. This occurs because behavioural traits, as well as the other typical components of the domestication phenotype (growth, stress, immune function, etc.), are most likely controlled by many genes, i.e. they are polygenic [15]. In addition, a given set of genes may influence different traits, a mechanism known as pleiotropy [42]. In such a case, increasing the frequency of alleles that, for example, up-regulate growth, may at the same time modify other essential welfare-related traits under the influence of the same genes. Finally, the function of one gene may also be influenced by the interaction with other genes, which is known as epistasis [43]. Selection for one or a few traits controlled by genes that have epistatic effects may thus influence a group of other genes, regulating other characters than those selected for. Therefore, both mechanisms (pleiotropy and epistasis) are more than likely to create side-effects on traits that are not desirable [15]. In fact, when animals are selected for production traits mainly, many side-effects have been extensively documented in several species [41]. Some of these side-effects will even affect production itself, such as reduced fertility in fast- growing broilers [41], and are likely to be the target of counter-selection. In other cases, the side-effects may be related to less-obvious traits which may nevertheless have a strong welfare aspect [44] because they shift welfare optima towards unknown directions. These processes have occurred in land animals throughout their domestication. However, the slow and long domestication process on land has allowed both humans and many livestock species to adapt and cope with such

from mutations, and that many genes must be involved [39, 40].

strategies, health status and farm management.

3.1. Genes

114 Animal Domestication

Changes in the phenotypes of selected farmed fish usually correlate with changes in physiological indicators. For example, when comparing seventh-generation farmed Atlantic salmon with wild individuals, the domesticated fish grow much faster (even more so in salt water where the difference is threefold), pituitary and plasma growth hormone levels were positively correlated with growth rate and significantly higher in the domesticated strain [45]. The same occurs with strains of Brook trout (Salvelinus fontinalis) farmed for 30 or more years (ca. 10 generations). The domesticated phenotype is less resilient than the wild, since hatchery-born fingerlings struggle to survive when released into native streams. Moreover, domesticated strains grow better in aquaculture but not in the wild [46], which led some authors to claim that domesticated animals are better adapted to captivity, reducing stress and mortality, increase disease resistance, reduce the use of chemotherapeutics and contribute to better animal welfare and environmental management. Up to 65% of farmed salmon in Norway comes from improved breeding plans, after an extensive programme lasting over 40 years and an enormous investment effort, with numbers reaching nine digits [26]. However, and despite these efforts and claims, 40 years represent only 10–13 generations of farmed salmon (Figure 1). Even more importantly, a recent analysis of welfare conditions of farmed salmon revealed a need for improvement in space, substrate, aggression, stress levels and malformations ([47], see Salmo salar). A possible conclusion is that the improvement programme of salmon in Norway may be focusing mostly on production-related traits. Although there are improvements on the health perspective of welfare, the natural needs and behaviour of this species in captivity may be generally impaired.

For many physiological indicators such as those listed below, selected strains of farmed fish fail to show positive results:

Metabolic rate: fast growing hatchery strains of Rainbow trout present higher standard metabolic rate (SMR), lower aerobic scope, and potentially lower maximum metabolic rates, suggesting that high growth trades off against a reduced capacity to do metabolic work. Higher SMR of fast growers appears to be related to a greater investment in high-maintenance digestive tissue that supports rapid growth, which appears to compromise active metabolism [48]. Farmed Senegalese sole (Solea senegalensis) born from wild spawners are nevertheless capable of shifting their routine metabolism from naturally nocturnal to diurnal, responding to daylight feeding regimes [49].

Hypoxia resistance: triploid strains of domesticated Rainbow trout show faster growth than wild diploid individuals probably due to impaired gametogenesis of 3n fish [50]. Adding to these reproductive problems, triploids are also less resistant to hypoxia [51], which can account for lesser resistance and higher mortalities both in nature [52, 53] and in several types of farming conditions and methods [54–57].

Stress: there are reports of selected strains of farmed fish showing lower stress responses to acute artificial stressors. In Rainbow trout, the cortisol responses to confinement in a net or to electroshock are higher in wild fish than in hatchery-reared animals [58]. However, there are also examples of the opposite pattern, even in the same species: wild trout show lower physiological stress responses to hooking than domesticated trout [59]. Immediate cortisol response to an acute handling stressor in a domesticated Eurasian strain of common carp is also higher than wild Japanese strain [60]. Although cortisol is a universally used indicator for stress, it should be used with caution. This hormone has an adaptive physiological role and several factors (e.g. genetic, developmental, environmental, frequency of exposure) underlie its release upon stressful episodes [61]. An appreciation of these factors, along with knowledge of the biology of the species, solid behavioural observations [16] and secondary stress indicators, such as plasma glucose and lactate [61], are essential for proper interpretation of the data and design of mitigation measures.

This may not only be due to a trade-off between brain size and reproduction [71], but also to the

Domestication and Welfare in Farmed Fish http://dx.doi.org/10.5772/intechopen.77251 117

Despite the consistency of the farming environment, different coping styles (e.g. consistent trait associations such as proactive, active coping or bold, and reactive, passive coping or shy) do emerge in farmed fish [72]. The proactive/reactive continuum has been identified in most farmed species and it should be a factor to consider when designing and evaluating production systems. However, the aquaculture industry selects mostly for growth performance [73] and proactive fish grow faster [74]. Consequently, there is a theoretical infinite selection for proactive and aggressive individuals in fish farming. This creates an obvious welfare problem that can only be solved by a deep understanding of the biology of the species as well as through the design of appropriate and diverse farming environments, which can accommodate different coping styles, even at the expense of lower production outputs [72]. In addition to coping styles, there is another source of intrinsic variability in animals that is phenotypic plasticity, best explained by behavioural reaction norms (BRN, i.e. the set of behavioural phenotypes that a single individual produces in a given set of environments) [75]. The BRN may actually be calculated, and it incorporates information on how an animal behaves on average and how its behaviour changes over a gradient, specifying the precise form of the relationship between response value and environmental condition. The relationships between food provisioning rate and begging intensity, between dispersal behaviour and current velocity, or between anti-predator behaviour and predation risk are all examples of BRNs. This approach treats both inter-individual and intra-individual variance in behaviour as meaning-

The implications of the domestication process on the behavioural perspective of welfare are therefore far from simple. Behavioural changes due to generations in captivity do seem to occur but (1) they are accompanied by physiological and cognitive modifications that are challenging to accommodate in good welfare, and (2) while the behavioural phenotypes of wild fish are adaptive and selected throughout stable evolutionary pressures, captive phenotypes are responding to extremely different settings that are artificially rapid and that can often

The available evidence, however, is largely based on data from salmonids. These species are nonetheless far from representing the majority of production of finfish in global aquaculture: Atlantic salmon ranks seventh in production worldwide with approximately 2.4 million tonnes in 2015 (less than half of the production of the #1, Grass carp (Ctenopharyngodon idella)

Fish are an extraordinary group of animals. Our 'underwater cousins', as Jonathan Balcombe describes them in his book What a fish knows [78], are the closest living relatives to our common aquatic ancestor. But, as with most distant family members, our understanding of their lives is limited. Even though ichthyology was incorporated as a formal science by Aristotle (383–322BC) [79], we still struggle to understand many aspects of fish biology. Those limitations to our knowledge of fish arise mainly from the fact that fish live in water. This posts a strong barrier

push welfare needs into collision with traits required for production.

lack of environmental challenges and corresponding cognitive selection pressures.

ful (rather than as 'noise') [76].

with 5.8 million tonnes) [77].

3.4. Sensory worlds

Overall performance: wild and hybrid (domesticated wild) strains of Brook trout showed better rates of recovery (from angling) and yield than a domestic strain [62]; wild strains of Nile tilapia (Oreochromis niloticus) perform as well as domesticated strains [63, 64]. Triploid strains of trout also generally tend to have higher malformation rates than wild populations [65].

From the available data on these indicators, it is not clear whether the current domestication process brings any obvious and effective physiological welfare benefits.

#### 3.3. Behaviour

As occurs with terrestrial farm animals, the environment experienced by cultured fishes highly differs from the wild [14, 66, 67]: the physical environment is much simpler, space is restricted, and migration is not possible; food is readily available so long distance tracking of food is unnecessary; there are generally fewer or no predators (apart from human), and they are treated for some diseases. For parent animals, reproduction occurs without the need to compete for mates as it is often the case in the wild. In these aspects, the environment is overall less challenging. In others, however, it is more challenging: fishes are frequently disturbed by human activity, they are usually confined at unnatural densities, which potentially increases the risk of infection and the incidence of social encounters, including aggressive ones, especially when competing for food. The hatchery environment is so different from that experienced in nature that it can potentially generate behavioural differences in three, interlinked ways: (1) differential experience, (2) differential mortality and survival of behavioural phenotypes within a single generation and (3) selection for inherited behavioural traits over several generations [68]. In fact, usual conditions in intensive husbandry favour risk-taking/aggressive fish, as available data suggests that competition for food is major driver for high-risk/high-aggression phenotypes [69]. Hatchery-reared fish are more prone to show higher risk-taking behaviour, which is directly linked with a higher risk of escapes from rearing systems (as in the case of sea cages) [70], and may severely decrease their chances of survival in the wild. Consequently, this leads to a wide range of welfare, environmental and economic consequences. Domesticated strains of guppies (Poecilia reticulata), which are not farmed for food but are nevertheless the object of strong artificial selection for aquarium hobbyists, tend to have smaller brains and less cognitive abilities. This may not only be due to a trade-off between brain size and reproduction [71], but also to the lack of environmental challenges and corresponding cognitive selection pressures.

Despite the consistency of the farming environment, different coping styles (e.g. consistent trait associations such as proactive, active coping or bold, and reactive, passive coping or shy) do emerge in farmed fish [72]. The proactive/reactive continuum has been identified in most farmed species and it should be a factor to consider when designing and evaluating production systems. However, the aquaculture industry selects mostly for growth performance [73] and proactive fish grow faster [74]. Consequently, there is a theoretical infinite selection for proactive and aggressive individuals in fish farming. This creates an obvious welfare problem that can only be solved by a deep understanding of the biology of the species as well as through the design of appropriate and diverse farming environments, which can accommodate different coping styles, even at the expense of lower production outputs [72]. In addition to coping styles, there is another source of intrinsic variability in animals that is phenotypic plasticity, best explained by behavioural reaction norms (BRN, i.e. the set of behavioural phenotypes that a single individual produces in a given set of environments) [75]. The BRN may actually be calculated, and it incorporates information on how an animal behaves on average and how its behaviour changes over a gradient, specifying the precise form of the relationship between response value and environmental condition. The relationships between food provisioning rate and begging intensity, between dispersal behaviour and current velocity, or between anti-predator behaviour and predation risk are all examples of BRNs. This approach treats both inter-individual and intra-individual variance in behaviour as meaningful (rather than as 'noise') [76].

The implications of the domestication process on the behavioural perspective of welfare are therefore far from simple. Behavioural changes due to generations in captivity do seem to occur but (1) they are accompanied by physiological and cognitive modifications that are challenging to accommodate in good welfare, and (2) while the behavioural phenotypes of wild fish are adaptive and selected throughout stable evolutionary pressures, captive phenotypes are responding to extremely different settings that are artificially rapid and that can often push welfare needs into collision with traits required for production.

The available evidence, however, is largely based on data from salmonids. These species are nonetheless far from representing the majority of production of finfish in global aquaculture: Atlantic salmon ranks seventh in production worldwide with approximately 2.4 million tonnes in 2015 (less than half of the production of the #1, Grass carp (Ctenopharyngodon idella) with 5.8 million tonnes) [77].

#### 3.4. Sensory worlds

Stress: there are reports of selected strains of farmed fish showing lower stress responses to acute artificial stressors. In Rainbow trout, the cortisol responses to confinement in a net or to electroshock are higher in wild fish than in hatchery-reared animals [58]. However, there are also examples of the opposite pattern, even in the same species: wild trout show lower physiological stress responses to hooking than domesticated trout [59]. Immediate cortisol response to an acute handling stressor in a domesticated Eurasian strain of common carp is also higher than wild Japanese strain [60]. Although cortisol is a universally used indicator for stress, it should be used with caution. This hormone has an adaptive physiological role and several factors (e.g. genetic, developmental, environmental, frequency of exposure) underlie its release upon stressful episodes [61]. An appreciation of these factors, along with knowledge of the biology of the species, solid behavioural observations [16] and secondary stress indicators, such as plasma glucose and lactate [61], are essential for proper interpretation of the data and

Overall performance: wild and hybrid (domesticated wild) strains of Brook trout showed better rates of recovery (from angling) and yield than a domestic strain [62]; wild strains of Nile tilapia (Oreochromis niloticus) perform as well as domesticated strains [63, 64]. Triploid strains of trout

From the available data on these indicators, it is not clear whether the current domestication

As occurs with terrestrial farm animals, the environment experienced by cultured fishes highly differs from the wild [14, 66, 67]: the physical environment is much simpler, space is restricted, and migration is not possible; food is readily available so long distance tracking of food is unnecessary; there are generally fewer or no predators (apart from human), and they are treated for some diseases. For parent animals, reproduction occurs without the need to compete for mates as it is often the case in the wild. In these aspects, the environment is overall less challenging. In others, however, it is more challenging: fishes are frequently disturbed by human activity, they are usually confined at unnatural densities, which potentially increases the risk of infection and the incidence of social encounters, including aggressive ones, especially when competing for food. The hatchery environment is so different from that experienced in nature that it can potentially generate behavioural differences in three, interlinked ways: (1) differential experience, (2) differential mortality and survival of behavioural phenotypes within a single generation and (3) selection for inherited behavioural traits over several generations [68]. In fact, usual conditions in intensive husbandry favour risk-taking/aggressive fish, as available data suggests that competition for food is major driver for high-risk/high-aggression phenotypes [69]. Hatchery-reared fish are more prone to show higher risk-taking behaviour, which is directly linked with a higher risk of escapes from rearing systems (as in the case of sea cages) [70], and may severely decrease their chances of survival in the wild. Consequently, this leads to a wide range of welfare, environmental and economic consequences. Domesticated strains of guppies (Poecilia reticulata), which are not farmed for food but are nevertheless the object of strong artificial selection for aquarium hobbyists, tend to have smaller brains and less cognitive abilities.

also generally tend to have higher malformation rates than wild populations [65].

process brings any obvious and effective physiological welfare benefits.

design of mitigation measures.

3.3. Behaviour

116 Animal Domestication

Fish are an extraordinary group of animals. Our 'underwater cousins', as Jonathan Balcombe describes them in his book What a fish knows [78], are the closest living relatives to our common aquatic ancestor. But, as with most distant family members, our understanding of their lives is limited. Even though ichthyology was incorporated as a formal science by Aristotle (383–322BC) [79], we still struggle to understand many aspects of fish biology. Those limitations to our knowledge of fish arise mainly from the fact that fish live in water. This posts a strong barrier for the direct observation of these animals, and up until recently the study of fish was restricted to investigation from the surface under particular conditions of water transparency and shallow depth, the examination of dead specimen or watching captive animals in artificial conditions. This constraint was only truly overcome with the invention of the self-contained underwater breathing apparatus by Jacques-Yves Cousteau and Emille Gagnan in 1942. Thus, only roughly 80 years ago could humans consistently observe fish in their natural habitats, in a similar way than we had been doing with terrestrial animals since the dawn of our species. This gap in the knowledge of fish biology is a major drawback for the establishment of welfare standards. Since self-experience and individual knowledge are impossible to be observed directly, their existence in other species tends to be forgotten or ignored, especially in taxa with which we do not readily identify or that are distantly related to us [80]. While we as humans can easily empathise with cattle, goats, sheep, horses and other terrestrial animals because they have been living next to us for millennia and share most of our sensory world, fishes exist in a realm of their own.

Chemical sensing in fish exists in three modalities: olfaction, solitary chemosensory cells and taste. Olfaction may function at a larger distance for all the roles described above, and olfactory receptors are usually located in the nostrils on the most anterior part of the head. Taste cells are usually limited to very close range detection of foodstuffs and are located in the head and mouth [85]. In most predatory fishes, the taste system is used solely during oral food evaluation [89]. Solitary chemosensory cells are not well described yet but may serve as food, predator or conspecific

Domestication and Welfare in Farmed Fish http://dx.doi.org/10.5772/intechopen.77251 119

In all fishes, sound is detected by one or more of the otolith organs. As sound passes through a fish and brings its tissues into motion, the otoliths respond to sound-induced motions of the animal's body. In many fish species, named hearing specialists, the otoliths may also receive a displacement input from the swimbladder or another gas-filled chamber near the ears. These fishes may respond to both acoustic pressure and particle motion with a particularly efficient coupling between the gas bladder and the otolith organs and tend to have very high sensitivity

In addition, fishes have evolved a diversity of sound-generating organs. These include vibrating the swimbladder and pectoral girdle or rubbing bony elements against each other. Sounds are produced in various behavioural contexts (agonistic interactions, courtship, spawning and in distress). Similarly to chemical communication, acoustic signals may serve in decreasing aggression, assessment of the fighting abilities, species recognition, mate attraction and mate choice [90].

The aquatic environment influences basic perception and adaptation to damage in fishes: for example, they cannot fall because of buoyancy in the water column and this prevents injury due to gravity; noxious chemicals entering the aquatic environment may be diluted and thus pose a lower risk; and major shifts in temperature are less common compared with terrestrial environments. This could mean fishes experience less risk of damage than terrestrial animals, and it may be reflected in their nociceptive system [81]. In fact, although receptors for damaging stimuli have been found in all fish groups, and fishes possess neuroanatomical pathways comparable to those found in other vertebrate groups, there are interesting differences that reveal adaptions to evolutionary pressures: for example, rainbow trout nociceptors are not activated in low temperatures, because they live in cold water [91], but they are more sensitive to mechanical stimuli than mammals, probably because their skin is more fragile, and to heat, probably because they live in temperatures usually not above to 25C [92]. The Chameleon cichlid (Australoheros facetus), on the other hand, is far more tolerant to heat exposure, which can also be explained by its broad ecological distribution [93]. Importantly, fish are ectothermic, and therefore their inner temperature depends on the environment (typically 0–30C). As mammals maintain homeostasis at 37C, it is likely that fish nociceptors have a lower temperature threshold than mammals [81]. Interestingly, the same groups of substances that reduce pain in humans (opioids, anti-inflammatory drugs and local anaesthetics) are also effective in reducing behavioural and physiological

indicators of discomfort in teleosts, which is indicative of similar sensing mechanisms [81].

locators, spread throughout the body of the animal [85].

3.4.3. Hearing

to sound [80].

3.4.4. Nociception

In fact, there are likely to be substantial differences in fish sensory systems compared with a terrestrial animal due to differing ecological and evolutionary pressures [81]. The term Umwelt was coined by Jakob von Uexküll in 1909 and refers to the sensory world of an animal—i.e. a subject—who is perceiving and actively responding to environmental stimuli. Moreover, the animal is not reacting mechanically to the world, and instead building its Umwelt with a meaningful living strategy, even though the behaviours may not be consciously planned [82]. This concept is of vital importance for the design of welfare solutions for captive fishes, because the sensory world of these animals differs highly from our own experience, is extraordinarily diverse, and relies on senses that differ from ours.

#### 3.4.1. Vision

Light behaves differently underwater than at the surface and can be influenced by physical and biological factors. Depth can modulate the wavelength (i.e. the colour), while intensity and scatter can be modified by turbidity and suspended particle type. These can also change rapidly with daytime, season or weather conditions. Furthermore, species have different visual systems depending on their life-history (e.g. predators that rely on visual cues for feeding, fishes that are common preys and must remain vigilant for evasion) or even within life stages (e.g. larvae that live in the depths and move to shallower depth when they grow, species with ocean juveniles and freshwater adults). These environmental changes represent huge selective pressures for the radiation of visual systems in fish. Not surprisingly, there is an enormous variety not only in the type of eyes that can be found in fish [83], but also in the brain structures that process visual information [84].

#### 3.4.2. Chemical sensing

Chemical senses serve an essential ecological role and are extremely relevant in communication contexts in all groups of fish (cyclostomes, elasmobranchs and teleosts). They enable orientation in the dark or blurry waters, predation, foraging and escape from predators for example [85]. Chemical sensing also serves intra-specific communication, allowing males and females to find suitable partners [86], as well as competitors to assess and announce their status in agonistic contexts, which are solved much quicker and less violently thanks to 'chemical diplomacy' [87, 88]. Chemical sensing in fish exists in three modalities: olfaction, solitary chemosensory cells and taste. Olfaction may function at a larger distance for all the roles described above, and olfactory receptors are usually located in the nostrils on the most anterior part of the head. Taste cells are usually limited to very close range detection of foodstuffs and are located in the head and mouth [85]. In most predatory fishes, the taste system is used solely during oral food evaluation [89]. Solitary chemosensory cells are not well described yet but may serve as food, predator or conspecific locators, spread throughout the body of the animal [85].

#### 3.4.3. Hearing

for the direct observation of these animals, and up until recently the study of fish was restricted to investigation from the surface under particular conditions of water transparency and shallow depth, the examination of dead specimen or watching captive animals in artificial conditions. This constraint was only truly overcome with the invention of the self-contained underwater breathing apparatus by Jacques-Yves Cousteau and Emille Gagnan in 1942. Thus, only roughly 80 years ago could humans consistently observe fish in their natural habitats, in a similar way than we had been doing with terrestrial animals since the dawn of our species. This gap in the knowledge of fish biology is a major drawback for the establishment of welfare standards. Since self-experience and individual knowledge are impossible to be observed directly, their existence in other species tends to be forgotten or ignored, especially in taxa with which we do not readily identify or that are distantly related to us [80]. While we as humans can easily empathise with cattle, goats, sheep, horses and other terrestrial animals because they have been living next to us

for millennia and share most of our sensory world, fishes exist in a realm of their own.

dinarily diverse, and relies on senses that differ from ours.

3.4.1. Vision

118 Animal Domestication

that process visual information [84].

3.4.2. Chemical sensing

In fact, there are likely to be substantial differences in fish sensory systems compared with a terrestrial animal due to differing ecological and evolutionary pressures [81]. The term Umwelt was coined by Jakob von Uexküll in 1909 and refers to the sensory world of an animal—i.e. a subject—who is perceiving and actively responding to environmental stimuli. Moreover, the animal is not reacting mechanically to the world, and instead building its Umwelt with a meaningful living strategy, even though the behaviours may not be consciously planned [82]. This concept is of vital importance for the design of welfare solutions for captive fishes, because the sensory world of these animals differs highly from our own experience, is extraor-

Light behaves differently underwater than at the surface and can be influenced by physical and biological factors. Depth can modulate the wavelength (i.e. the colour), while intensity and scatter can be modified by turbidity and suspended particle type. These can also change rapidly with daytime, season or weather conditions. Furthermore, species have different visual systems depending on their life-history (e.g. predators that rely on visual cues for feeding, fishes that are common preys and must remain vigilant for evasion) or even within life stages (e.g. larvae that live in the depths and move to shallower depth when they grow, species with ocean juveniles and freshwater adults). These environmental changes represent huge selective pressures for the radiation of visual systems in fish. Not surprisingly, there is an enormous variety not only in the type of eyes that can be found in fish [83], but also in the brain structures

Chemical senses serve an essential ecological role and are extremely relevant in communication contexts in all groups of fish (cyclostomes, elasmobranchs and teleosts). They enable orientation in the dark or blurry waters, predation, foraging and escape from predators for example [85]. Chemical sensing also serves intra-specific communication, allowing males and females to find suitable partners [86], as well as competitors to assess and announce their status in agonistic contexts, which are solved much quicker and less violently thanks to 'chemical diplomacy' [87, 88].

In all fishes, sound is detected by one or more of the otolith organs. As sound passes through a fish and brings its tissues into motion, the otoliths respond to sound-induced motions of the animal's body. In many fish species, named hearing specialists, the otoliths may also receive a displacement input from the swimbladder or another gas-filled chamber near the ears. These fishes may respond to both acoustic pressure and particle motion with a particularly efficient coupling between the gas bladder and the otolith organs and tend to have very high sensitivity to sound [80].

In addition, fishes have evolved a diversity of sound-generating organs. These include vibrating the swimbladder and pectoral girdle or rubbing bony elements against each other. Sounds are produced in various behavioural contexts (agonistic interactions, courtship, spawning and in distress). Similarly to chemical communication, acoustic signals may serve in decreasing aggression, assessment of the fighting abilities, species recognition, mate attraction and mate choice [90].

#### 3.4.4. Nociception

The aquatic environment influences basic perception and adaptation to damage in fishes: for example, they cannot fall because of buoyancy in the water column and this prevents injury due to gravity; noxious chemicals entering the aquatic environment may be diluted and thus pose a lower risk; and major shifts in temperature are less common compared with terrestrial environments. This could mean fishes experience less risk of damage than terrestrial animals, and it may be reflected in their nociceptive system [81]. In fact, although receptors for damaging stimuli have been found in all fish groups, and fishes possess neuroanatomical pathways comparable to those found in other vertebrate groups, there are interesting differences that reveal adaptions to evolutionary pressures: for example, rainbow trout nociceptors are not activated in low temperatures, because they live in cold water [91], but they are more sensitive to mechanical stimuli than mammals, probably because their skin is more fragile, and to heat, probably because they live in temperatures usually not above to 25C [92]. The Chameleon cichlid (Australoheros facetus), on the other hand, is far more tolerant to heat exposure, which can also be explained by its broad ecological distribution [93]. Importantly, fish are ectothermic, and therefore their inner temperature depends on the environment (typically 0–30C). As mammals maintain homeostasis at 37C, it is likely that fish nociceptors have a lower temperature threshold than mammals [81].

Interestingly, the same groups of substances that reduce pain in humans (opioids, anti-inflammatory drugs and local anaesthetics) are also effective in reducing behavioural and physiological indicators of discomfort in teleosts, which is indicative of similar sensing mechanisms [81].

#### 3.4.5. Other senses

There are sensory systems in fish that are completely alien to us. The lateral line for example, which serves as a receptor for hydrodynamic stimuli such as those generated by conspecifics, predators or prey. Although the biological processing of hydrodynamic signals has been well studied, not much is known about how fish can discern these from natural occurring events [94]. As all fishes experience night, darkness or turbid waters, there is strong selection for the use of non-visual senses in all fish species. Anatomical diversity suggests that the lateral line is one of the most important senses for fishes. However, research on the function of the lateral line has lagged due to poor understanding of hydrodynamics at small scales and lack of this sense in humans, making it difficult to imagine a fish's hydromechanical world [95]. Electrical sensing is ancestral to fishes and is present in most non-teleosts as well as certain teleost species. The electrosensory world of fishes is rich with electric fields from a multitude of sources including the earth's magnetic field and the bodies of all aquatic organisms including the electrosensing fish itself. The fish's extremely high sensitivity to these fields enables orientation, navigation, communication, and even detection and localization of other fish, both prey and conspecifics [96–98]. Figure 2 summarises the sensory world of fish.

understanding of fish locomotion, and the design of appropriate rearing systems. The 3D nature of fish functional design is clearly demonstrated in the enormous diversity of body

Domestication and Welfare in Farmed Fish http://dx.doi.org/10.5772/intechopen.77251 121

Other physical properties of water affect fish in a different way than dry land does to farm animals: for example, water is a dense medium, so fish are constrained by hydrodynamic demands and fast swimming can be costly; gases dissolve readily in water, but moving water for oxygen extraction is energetically costly; many other chemicals readily dissolve and dis-

In order to adapt to such a different medium, fishes not only develop the extraordinary sensory systems we have discussed above, but also show many amazing morphological and physiological adaptations, that can strongly determine welfare needs: they may undergo dramatic changes in form and function across life stages, as in the case of flatfishes [100]; unlike mammals but in common with birds, fish red blood cells are nucleated, giving them additional functions including immune responses [68]; fish grow continuously [101], influencing their relation with space and density across time; most species excrete ammonia (which is highly toxic, especially in aquaculture conditions [102]) while land animals excrete urea [103]. Finally, fish have more genes, more gene variability and more gene duplicates

To summarise, the extraordinary features of the aquatic environment, the exotic adaptations of fish and their Umwelt represent a challenge for the assessment of fish welfare. Only through a deep understanding not only of the fundamental differences between fish and terrestrial farm animals but also of the specific needs of each species can we design appropriate measures to improve and establish high standards of welfare in aquaculture. This task becomes even more daunting considering the number of animal species currently being farmed in aquatic environments: 362 finfishes (including hybrids), 104 molluscs, 62 crustaceans, 6 frogs and reptiles, and 9 aquatic invertebrates [106]. For the sake of comparison, there are 26 well-studied species of terrestrial farm animals, according to the Domestic Animal Diversity Information System (DAD-IS) [107]. Due to their low number of species, welfare measures and standards are easier to establish for land animals than for fishes. With such a long list of fish species in current

world farming, how to tackle the issue of assessing fish welfare in a global manner?

Welfare in aquaculture has been a motive of academic work in the recent past. Several authors have addressed the topic in reviews and research papers [16, 68, 108–110], and the COST action Welfare of fish in European aquaculture has been promoted aiming to (i) improve the knowledge on welfare of fish, (ii) formulate a set of guidelines embodying a common and scientifically sound understanding of the concept of welfare in farmed fish, and (iii) construct a range of targeted operational welfare indicator protocols to be used in the industry [111]. The results of this action were incorporated in many research projects, not only in Europe but also in the USA, Canada, and New Zealand. In addition, major stakeholders in the industry were also

shapes and swimming modes in fishes [99].

than terrestrial animals [104, 105].

4. Assessing welfare in farmed fish

perse in water.

Not only the sensory world of fishes is difficult to relate to, but also the physics of movement underwater in a three-dimensional world can be challenging to understand for humans, who exist roughly in a 2D world. Despite this challenge, it is nonetheless a critical next step for the

Figure 2. The sensory worlds of fish.

understanding of fish locomotion, and the design of appropriate rearing systems. The 3D nature of fish functional design is clearly demonstrated in the enormous diversity of body shapes and swimming modes in fishes [99].

Other physical properties of water affect fish in a different way than dry land does to farm animals: for example, water is a dense medium, so fish are constrained by hydrodynamic demands and fast swimming can be costly; gases dissolve readily in water, but moving water for oxygen extraction is energetically costly; many other chemicals readily dissolve and disperse in water.

In order to adapt to such a different medium, fishes not only develop the extraordinary sensory systems we have discussed above, but also show many amazing morphological and physiological adaptations, that can strongly determine welfare needs: they may undergo dramatic changes in form and function across life stages, as in the case of flatfishes [100]; unlike mammals but in common with birds, fish red blood cells are nucleated, giving them additional functions including immune responses [68]; fish grow continuously [101], influencing their relation with space and density across time; most species excrete ammonia (which is highly toxic, especially in aquaculture conditions [102]) while land animals excrete urea [103]. Finally, fish have more genes, more gene variability and more gene duplicates than terrestrial animals [104, 105].

To summarise, the extraordinary features of the aquatic environment, the exotic adaptations of fish and their Umwelt represent a challenge for the assessment of fish welfare. Only through a deep understanding not only of the fundamental differences between fish and terrestrial farm animals but also of the specific needs of each species can we design appropriate measures to improve and establish high standards of welfare in aquaculture. This task becomes even more daunting considering the number of animal species currently being farmed in aquatic environments: 362 finfishes (including hybrids), 104 molluscs, 62 crustaceans, 6 frogs and reptiles, and 9 aquatic invertebrates [106]. For the sake of comparison, there are 26 well-studied species of terrestrial farm animals, according to the Domestic Animal Diversity Information System (DAD-IS) [107]. Due to their low number of species, welfare measures and standards are easier to establish for land animals than for fishes. With such a long list of fish species in current world farming, how to tackle the issue of assessing fish welfare in a global manner?
