fish cognition and behavior (brown/fish cognition and behavior) || cognition and welfare

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Chapter 17 Cognition and Welfare Lynne U. Sneddon 17.1 Introduction There has been a tremendous growth in scientific studies addressing fish welfare questions over recent years. These studies provide clear evidence for fish experiencing ‘negative’ welfare states such as pain, fear and stress (Conte 2004; Sneddon 2006; Ashley 2007; Ashley & Sneddon 2007; Sneddon 2009). However, there has also been much controversy and debate as to whether fishes are consciously aware of these complex emotions due to their smaller brain size and lack of a neocortex (Section 17.2; Rose 2002; Iwama 2007). These reviewers also suggest that fishes are stimulus-response beings lacking any thought processing or decision-making; are incapable of any complex learning and memory; and are restricted to simple forms of learning such as non-associative learning and classical conditioning (Rose 2002; Iwama 2007). The preceding chapters in this book have detailed a myriad of advanced behaviours reliant upon recognition of external biotic factors including profitable prey and danger in the form of predatory threat; differentiating conspecifics to identify suitable mates (Chapter 5) and discrimination of kin from non-kin (Chapter 9); adopting adaptive behaviours in others through social learning (Chapter 11); learning to avoid aversive stimuli (Chapters 15 and 16); and recall of navigation routes (Chapter 8). Much of this information must be learned and remembered to make behavioural decisions that improve survivorship and ultimately fitness. Fishes are also capable of modulating their social behaviour through prior experience (Chapter 11) and engage in complicated inter- specific and intraspecific relationships that involve cooperation and reciprocation (Chapter 12). The subjects in these social relationships, in most instances, will only engage with others when it is in their own best interest as clearly illustrated by specific examples of manipulation of others (Chapter 13). Such advanced behaviours were thought to occur only in mammals and possibly birds, but due to clever experimental approaches we are now beginning to understand that cognition and so-called higher mental functions do occur in fishes even with their relatively smaller brains and less differentiated cortex (Section 17.2). Current research has shown that fishes have clear preferences for particular items and resources, exhibit mate choice, favour social interactions with related individuals and select the most preferable environmental conditions (Section 17.3). Conversely, fishes also Fish Cognition and Behavior, Second Edition. Edited by Culum Brown, Kevin Laland and Jens Krause. C 2011 Blackwell Publishing Ltd. Published 2011 by Blackwell Publishing Ltd.

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BLBK374-17 BLBK374-Brown May 13, 2011 17:37 Copyeditor’s Name: Trim: 244mm X 172mm Char Count=

Chapter 17

Cognition and Welfare

Lynne U. Sneddon

17.1 Introduction

There has been a tremendous growth in scientific studies addressing fish welfare questionsover recent years. These studies provide clear evidence for fish experiencing ‘negative’welfare states such as pain, fear and stress (Conte 2004; Sneddon 2006; Ashley 2007;Ashley & Sneddon 2007; Sneddon 2009). However, there has also been much controversyand debate as to whether fishes are consciously aware of these complex emotions due totheir smaller brain size and lack of a neocortex (Section 17.2; Rose 2002; Iwama 2007).These reviewers also suggest that fishes are stimulus-response beings lacking any thoughtprocessing or decision-making; are incapable of any complex learning and memory; andare restricted to simple forms of learning such as non-associative learning and classicalconditioning (Rose 2002; Iwama 2007). The preceding chapters in this book have detailed amyriad of advanced behaviours reliant upon recognition of external biotic factors includingprofitable prey and danger in the form of predatory threat; differentiating conspecifics toidentify suitable mates (Chapter 5) and discrimination of kin from non-kin (Chapter 9);adopting adaptive behaviours in others through social learning (Chapter 11); learning toavoid aversive stimuli (Chapters 15 and 16); and recall of navigation routes (Chapter 8).Much of this information must be learned and remembered to make behavioural decisionsthat improve survivorship and ultimately fitness. Fishes are also capable of modulating theirsocial behaviour through prior experience (Chapter 11) and engage in complicated inter-specific and intraspecific relationships that involve cooperation and reciprocation (Chapter12). The subjects in these social relationships, in most instances, will only engage withothers when it is in their own best interest as clearly illustrated by specific examples ofmanipulation of others (Chapter 13). Such advanced behaviours were thought to occuronly in mammals and possibly birds, but due to clever experimental approaches we arenow beginning to understand that cognition and so-called higher mental functions do occurin fishes even with their relatively smaller brains and less differentiated cortex (Section17.2). Current research has shown that fishes have clear preferences for particular itemsand resources, exhibit mate choice, favour social interactions with related individuals andselect the most preferable environmental conditions (Section 17.3). Conversely, fishes also

Fish Cognition and Behavior, Second Edition. Edited by Culum Brown, Kevin Laland and Jens Krause.C© 2011 Blackwell Publishing Ltd. Published 2011 by Blackwell Publishing Ltd.

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406 Fish Cognition and Behavior

display strong aversive responses and avoid unfavourable items, conspecifics and habitatconditions (Section 17.4). These studies provide an insight into what choices fishes maymake through cognitive testing. Moreover, this review outlines the accumulating evidencethat fishes experience pain and fear in a similar manner to other vertebrates (Section 17.5).These findings have significant implications for fish welfare (Section 17.2) and raise a con-siderable number of controversial questions (Section 17.7). For example, how should fishesbe killed in commercial fishing operations? Is recreational fishing morally defendable?Should aquarium owners be licensed? The strict welfare and ethics regulations that areapplied to mammals, birds and reptiles have not been routinely applied to fishes. The timeis rapidly approaching when legislation regarding fish welfare will need to be revisited.

17.1.1 Fish welfare

Fishes are the third most popular experimental model in the United Kingdom afterrats and mice (APC, UK, http://apc.homeoffice.gov.uk/reference/apc-05-26.pdf) and inAustralia fishes comprise approximately 80% of all study animals subject to licensedscientific procedures. Indeed, over the last 12 months 10% of all animal behaviourpublications in internationally peer-reviewed journals use fishes as model organisms(Brown personal communication). Fishes are an important source of protein with overhalf a million tonnes of fishes produced by aquaculture in Europe (FEAP, http://www.feap.info/feap/presentations/EUparliament en.asp) annually and approximately 73 milliontonne of fishes caught in marine waters globally (FAO 2006). Finally, in developed nations,fishes are the third most popular pet after dogs and cats although they easily outnumbernumber them in absolute terms (Iwama 2007). Thus, fishes play significant roles in ourlives and the way in which we interact with them warrants careful thought if they arecapable of experiencing negative affective states and, as a consequence, suffer. Not onlyshould we consider minimising adverse emotional states but we should also seek to caterfor increasing positive experiences. For example, what does a fish of a given species wantor need within its aquarium to allow it to freely express its normal behavioural repertoire?Cognitive approaches can inform us as to what animals prefer, avoid and what particularinternal or mental states are important to the individual. Understanding the subjective andemotional lives of animals should enable us to improve fish welfare.

Emotions in fishes are not as apparent as in mammals making such study problem-atic. Fishes do not audibly vocalise (although they can be heard only with special soundequipment) nor do they have recognisable facial expressions linked to positive or negativeaffective states. However, this lack of an overt and recognisable response does not precludethe possibility that fishes have emotions. A variety of studies have produced significant datademonstrating fear in fishes (Yue et al. 2004; Ashley & Sneddon 2007; Sneddon 2009).While fishes may lack obvious facial expressions, they do exhibit subtle changes in finposture and colouration that can be readily linked to a variety of states such as disease,fear and stress (Gibson et al. 2009; Korsoen et al. 2009). Species-specific responses to apotentially painful event have been identified (Reilly et al. 2008), so the welfare contextand interspecific variation should be considered. More research is needed to clearly identifyand characterise reliable indictors that can be easily assessed visually when determiningfish welfare.

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Opinions regarding the status of fish cognition are divided with some authors suggestingthat fishes lack cognitive and decision-making processes (Rose 2002; Iwama 2007) andmany are unwilling to apply the capacity for experiencing even basic emotions to fishes dueto morphological and neuroanatomical differences. In comparison, other aquatic animals,such as cetaceans, are readily accepted as being second to humans in their cognitive ability.The rules of evolution dictate that no function suddenly arises in an animal group withoutthat function evolving in ancestral animals. Therefore, cognitive functions and emotionalexperiences should be considered on a phylogenetic sliding scale (Bekoff & Sherman 2004);humans in this case may have the most advanced cognition and fishes, in comparison, maybe considered more rudimentary, but as we have read in the preceding chapters, certainlynot lacking in cognitive power entirely. In Section 17.5, studies demonstrating pain and fearin fishes are discussed in terms of what these data tell us about cognition and welfare.

17.1.2 Preference and avoidance testing

Using preference and avoidance testing, we can gain a better understanding of what animalsprefer as well as identifying stimuli that are avoided (Section 17.3). Informed decisions onpositive and negative ‘feelings’ or improving welfare can be made based upon the prefer-ences and avoidance decisions made directly by an animal (Bekoff 2006, 2007). There aremany examples of fishes in their natural habitat displaying preferences for specific temper-atures, oxygen levels, habitat types and other abiotic factors (Fangue et al. 2009; Ludsinet al. 2009; Plumb & Blanchfield 2009). Extrapolating from natural habitat preferencescan assist in advising the optimum environmental conditions in which to hold these speciesin captivity. These conditions can be modified further by using preference tests. Reliablepreference data is vital to understand what choices are made by the animal and is indicativeof the fact that access to a specific resource is rewarding or beneficial (McMillan & Lance2004; Balcombe 2006; Bekoff 2006). For example, iguanas prefer a warm environmentwith no food rather than experiencing cold conditions where food is available (Ramirez &Cabanac 2003). Thus, preference testing provides an insight into what animals want or needand the rank order of importance. In other experimental paradigms, one can examine howmuch effort they are willing to expend to obtain desirable resources (Carbone 2004). Thislatter approach involves the animal paying a cost to accessing resources that they value.The effort extended to gain access to the resource can be used as a form of standardisedcurrency. Studies in pigs and mink have used these approaches where, for example, increas-ing weights were applied to doors that provided access to water. The heavier the weightthe more effort must be spent on gaining access to the resource and thus the researcher isable to determine how much the animal will work to obtain access to the water. Similarly,one can train animals to press a lever to gain access to a resource and the number of leverpresses required to unlock the door can be progressively increased. This type of testing hasnot been applied to fishes but obviously could tell us how much a fish would be willing topay in order to obtain a preferred resource.

Avoidance testing, in contrast, demonstrates how important aversive stimuli are to ananimal (Section 17.4). If the subject quickly learns to avoid a situation or event, then thisis one that may have a negative impact on welfare. The animal may be so highly motivatedby this adverse experience that it acquires an avoidance response after just one trial or

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exposure. Examples of such stimuli are nearly always obviously aversive including electricshock or fear-eliciting paradigms. Learning after a single exposure to a potentially damagingevent such as hooking during capture (Chapter 16) or predators (Chapter 3) provides clearevidence of the importance of these negative events to the animal.

17.1.3 Behavioural flexibility and intraspecific variation

With fishes being the most diverse vertebrate group, there will obviously be species dif-ferences in what fishes need in terms of habitat content as well as differences in how theydisplay negative emotions. Currently, studies on welfare in fishes are limited to a handfulof species; therefore, it is not possible to discuss large-scale group-specific requirementssuch as comparing cyprinids and gadoids with salmonids. Instead, a discussion on intraspe-cific variation in behavioural reactions highlights the argument against fishes being simplystimulus-response automatons. If fishes do lack the ability to be flexible in their responseand use only reflexive behaviour, then it is difficult to explain why we see individual vari-ation or ‘personality’ traits within a species (Wilson et al. 1993; Chapter 7). Personality,in philosophical terms, is not restricted to humans but is defined as the characteristics ofan individual that makes the individual distinct from another and thus recognisable. Whenapplied to fishes, personality is often expressed in multiple dimensions such as boldness,the propensity to take risks in the face of novel challenges (e.g. Brown et al. 2005; Frostet al. 2007). Fishes in wild and captive situations often have a dichotomous distributionconsisting of individuals showing bold, risky behaviours or conversely shy, cautious be-haviours. These intraspecific differences are also discussed with relevance to welfare andcognition in Section 17.6.

17.2 What is welfare?

Animal welfare has a number of definitions depending upon how one perceives what goodwelfare is. The meaning and definition of animal welfare and how best to objectivelymeasure it are subject to much discussion among scientists (Broom 1991a, 1991b; Dawkins1998a; Mendl & Paul 2004; Broom 2007). There are three main definitions:

(1) Good biological functioning is an accepted means of measuring welfare and unques-tionably provides scientific data regarding the physical condition of the animal. Poorhealth can be caused by, and may be a consequence of, suboptimal welfare, which canbe reliably quantified.

(2) The ‘feelings’-based definition of animal welfare goes beyond physical parameters andincludes a psychological component. This assumes that animals are sentient and havesubjective experiences and so can experience suffering on an emotional level (Broom1991b).

(3) Finally, ‘nature’-based concepts of animal welfare suggest that animals should be ableto freely perform their natural behavioural repertoire.

It is impossible to know if animals are aware of their emotions and consciously suffersince one would have to be an animal and know exactly how it feels. Indeed, we only know

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how other humans feel because they are able to communicate their experience. Therefore,many welfare scientists recommend that we should apply the precautionary principle andthat fishes should be given the benefit of the doubt and treated as if they do suffer (Bateson1991; Broom 1991a, 2007; Bekoff & Sherman 2004; Mendl & Paul 2004; Balcombe 2006;Arlinghaus et al. 2007, 2009; Bekoff 2007; Sneddon 2009). However, we can scientificallyand objectively measure responses to a painful event and use analgesics to return behaviourback to normal (Sneddon 2003a; Sneddon et al. 2003a) to prove that there are deleteriouschanges in fish behaviour that are alleviated by the administration of analgesia. There isgrowing evidence from scientific studies that make a robust case for fishes perceiving painand that this is an important and detrimental state for them to experience (Sneddon 2009).

Well-being is a term often used interchangeably with welfare and can be defined as thestate or condition of being well and content. From a well-being perspective, animals shouldbe disease free, kept in optimum conditions (if we have identified what these are) and befree from pain or suffering. This not only requires the use of analgesia and anaesthesia tominimise pain during invasive procedures but also being able to assess pain in animals.

17.2.1 Sentience and consciousness

For animals to have poor welfare or well-being, it is assumed they are at least sentientbeings. Sentience and consciousness have many definitions due to their complex natureand are readily debated amongst scientists and philosophers. Here, I define sentience as theability to detect and respond to external stimuli and having an awareness of pain, fear andstress (Dawkins 1998b; Broom 2007). Consciousness can be defined as an internal mentalimage and a sense of ‘I’ and how ‘I’ relate to the world (Beckoff & Sherman 2004). A varietyof studies have demonstrated that animals can detect and respond to painful stimuli (e.g.receptors, nociceptors that can detect noxious stimuli with subsequent changes in behaviourand physiology; Sneddon 2002; Sneddon 2003b; Sneddon et al. 2003b; Ashley et al. 2006,2007, 2009; Reilly et al. 2008), but the crucial point is whether these animals are consciousof the painful stimulus (i.e. do they know that they are in pain and hence suffer?). Doanimals have conscious thoughts where they relate to their own experience and think aboutthis in their minds? Some suggest that non-primate animals lack the cognitive abilities ofconscious beings because human conscious thought arises in the neocortex and, therefore,animals that lack a neocortex do not consciously experience the affective states of pain (Rose2002). If one accepts this opinion, then this means mammals such as dogs, cats, rodents aswell as birds and amphibians are also not aware of the negative affective component of painyet there is a plethora of published studies demonstrating that pain is an adverse experiencefor these animals (Gentle 1992; Flecknell et al. 2007). However, this opinion defies thelaws of evolution that suggests that each function has an evolutionary history that can betraced back in related taxa (Bekoff & Sherman 2004; Bekoff 2007). Moreover, animalswith a completely different life history, ecology and evolutionary trajectories may evolvethe same functions in completely different areas of the brain. This concept has already beendemonstrated in the avian and fish brains (Jarvis et al. 2005; Chapter 16). Therefore, it maynot be valid to attribute a function such as being consciousness to a particular brain areawhen comparing humans with other animals (Molyneux 2010).

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410 Fish Cognition and Behavior

It is impossible to measure emotion directly in any animal (including humans); therefore,the indirect evidence used to establish conscious motivational affective states must comefrom the study of neuroanatomy, neurophysiology and particularly behaviour (Duncan2002; Sneddon 2004, 2009).

17.2.2 Cognition and welfare

Specific types of behaviour are thought to be indicative of an animal’s ability to form internalrepresentations and act upon these depictions of its internal and external environments. Thisstate of basic or rudimentary consciousness is only thought to have been achieved in speciesthat have nervous systems that have attained a sufficient level of complexity during evolution(Shettleworth 2001). Therefore, cognitive studies of an animal may be used to assessconsciousness and sentience. Self-recognition is one of the key criteria for consciousness.There is evidence that fishes can indeed recognise themselves and discriminate themselvesfrom others, which was previously thought to be restricted to mammalian species. Thecichlid, Pelvicachromis taeniatus, recognises its own odour and prefers this over the odourof other fishes regardless if they are familiar or related (Thunken et al. 2009). To be able toengage in self-assessment of one’s own status and make behavioural decisions based uponthis, fishes must be able to compare themselves to others. Evidence from studies wherefishes watched conspecifics fight suggests that fishes are capable of making third-partyassessments of themselves relative to others since their performance is affected when facedwith the victor or loser of the observed interaction (Oliveira et al. 1998). These data suggestthat fishes are capable of self-recognition and self-assessment, which are central conceptsin higher cognitive processing and consciousness.

If fishes have cognitive functioning to such a degree that they exhibit clear preferences,avoid aversive stimuli, use tools (Pasko 2010), are able to learn complex tasks and havelong-term memory (Chapters 8, 11, 15 and 16), then this infers that they have some form ofinternal decision-making process as well as the capacity to remember negative events thatimpact upon their welfare. When considered in conjunction with the emerging evidencefrom behavioural studies that fishes are likely to have some form of consciousness and,therefore, may suffer on an emotional level, it is apparent that fish welfare becomes animportant issue. A greater understanding of the cognitive functioning of fishes providesus with insight into what they may experience when their welfare is compromised. Whilefurther research is clearly required, it is apparent that fishes have the capacity for painand suffering and this ought to be addressed whenever it is encountered. Therefore, it isvital to minimise or avoid procedures that cause pain, fear or stress to fishes to ensuregood welfare. However, positive welfare should also be enhanced rather than just tryingto minimise aversive events. Providing the ideal habitat in captivity might be a first stepin addressing these issues and determining what fishes need can be revealed by usingpreference tests (Section 17.3).

17.3 What fishes want

Concepts such as the five freedoms proposed for farmed animals are usually applied to allcaptive situations where animals are held by humans (FAWC 1996). These are (1) freedom

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from hunger and thirst, (2) freedom from environmental challenge, (3) freedom fromdisease, fear, pain, injury and discomfort, (4) freedom from behavioural restriction to allowexpression of the normal repertoire and (5) freedom from mental suffering. Therefore,when applying these freedoms to fishes, we require an understanding of how they areaffected when they are subject to these factors. Fishes are undoubtedly capable of makingdecisions in a variety of contexts and this may involve cognitive processing to varyingextents. The preference approach provides a reliable indicator of what a fish wants bymeans of exposing them to a choice test. This is based upon the premise that a sentientanimal would choose a beneficial option over one that is less beneficial or has a negativeimpact upon welfare. Therefore, the choice they make presumably has a perceived benefitover the alternative. However, this assumption may not always hold true. When given achoice between fruit and chocolate, for example, a child may choose chocolate even thoughit is not the most appropriate dietary item. Caution should be taken since the preferencedepends upon what choices are presented to the fish and could be significantly affectedby internal or physiological state at that time. Carefully designed experimentation shouldaccount for individual variation in sex, age, breeding condition and so on and also to pairspecific resources with one another so that a hierarchy of needs can be ascertained.

Preference tests must be designed to have biological relevance and, owing to theidiosyncrasies of various species, extrapolation between species is not always advisable.For example, a highly territorial species such as rainbow trout, Oncorhynchus mykiss,thrives in isolation from others whereas a sociably species such as common carp, Cyprinuscarpio, do not fare well when kept alone. Large groups of schooling or shoaling species,such as the zebrafish, Danio rerio, show little aggression but when held in smaller groups offour or less, significant amounts of aggression results in stress in subordinate individuals.Therefore, social groupings must be carefully differentiated between gregarious andterritorial species (Wirtz & Davenport 1976; Volpato et al. 2007). Therefore, with carefuldesign preference data can be extremely valuable in understanding the subjective needs offishes and can be applied to captive husbandry in terms of space requirements and usage,diet and time of feeding, light regime and intensity, oxygenation, temperature, socialcontext, water quality and so on.

17.3.1 Preference tests

17.3.1.1 Physical habitat

There are many studies demonstrating preference for favourable environmental conditionsin a variety of fish species. Using observations from the wild environment, Sessa et al.(2008) designed an experiment to alter depth gradient in tanks of reproducing zebrafish toreflect natural conditions. Natural populations of zebrafish spawn in the shallows of waterbodies, which contrasts with captive conditions where they are expected to spawn in thedeepest area at the bottom of a tank. By providing a depth gradient, mating behaviour wasunaffected but ovoposition did occur in shallower depths with a significant increase in thenumber of embryos deposited and surviving compared with standard conditions (Sessaet al. 2008). This demonstrates that provision of a depth gradient can improve reproductivesuccess. Other examples include laboratory-held weakfish, Cynoscion regalis, who only

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412 Fish Cognition and Behavior

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Fig. 17.1 (a) The percentage of weakfish choosing the higher dissolved oxygen when given a choice between 1versus 2 mg/L (1 vs. 2); 2 versus 4 mg/L (2 vs. 4) and 4 versus 6 mg/L (4 vs. 6). (Adapted from Stierhoff et al. 2009;*P < 0.05.) (b) Mean ± SD percentage of Arctic charr under, on or out of shelter during development expressedin days post-fertilisation (dpf), significantly different fish locations (P < 0.05) are represented by a different letterabove the bar (Benhaim et al. 2009). (c) Mean amount of time(s) ±1 SE that intertidal fish fed on low-nutritionalgae (black bar) and on higher nutrition bivalves (white bar) stayed at low-, intermediate- and high-temperaturecells of the thermal gradient. Total duration of each trial (fish) was 60 minutes, and 11 replicates were conductedper experimental group (Pulgar et al. 2003). (d) Mean amount of time(s) ±1 SE that individually housed brownstriped female fighting fish spent when presented with a choice of five white fishes (5W) versus five brown fishes(5B) and a choice of five brown fishes (5B) versus one brown fish (1B). (*P < 0.05.) (Adapted from Blakesleeet al. 2009. All figures are reproduced by kind permission from Elsevier.)

avoid low oxygen concentrations that negatively affect their growth rate and demonstrateno preference between oxygen levels that appear to have no impact on their physiology(Stierhoff et al. 2009; Fig. 17.1a). In broad-nosed pipefish, Syngnathus typhle, broodingmales chose to spend more time in higher temperature areas of an aquarium than females,the latter of which exhibited no preference (Ahnesjo 2008). This behavioural temperaturepreference could be linked to increased male brooding rate. Reproductive status also af-fected temperature preference in Japanese eels, Anguilla japonica, where they choose tospawn in temperatures of 18◦C–22◦C in captivity, similar to ambient temperatures, whengiven a choice ranging between 14◦C and 27◦C (Dou et al. 2008). When given a rangeof salinities, temperatures and substrates to choose from, the mudskipper, Boleophthalmuspectinirostris, exhibited profound preferences for approximately 31◦C, salinity of 5 ppm andsandy mud substrate which governs this species’ choice of microhabitat (Chen et al. 2008).

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Habitat composition can have dramatic effects on the biological functioning of fisheswith positive implications for welfare. Arctic charr, Salvelinus alpinus, when reared frombirth with a shelter in their tanks exhibited better growth, lower mortality and commencedfirst feeding about 6 days later compared with fishes without shelter (Benhaim et al. 2009;Fig. 17.1b). This study also adopted preference tests during development and found that ahigher proportion of fishes used the shelter rather than being visible in the open.

The animals in these studies based their choice upon the relative value of the resourcesto which they were exposed. The animal must judge its preferred choice to be better thanthe alternative and this provides some insight into what fishes want and need in theirenvironment. These studies provide clear preferences that are species specific and that canbe used to inform guidelines as to the captive husbandry of fish species in terms of physicalenvironmental and ecological conditions.

17.3.1.2 Breeding

Many animals including fishes construct nests for breeding purposes. For example, malesticklebacks build elaborate nests in the breeding season and females use this to judge malequality and to decide which male to mate with (Rushbrook et al. 2008). The female laysher eggs within the nest and the male fertilises them and performs parental care until theeggs hatch. Many captive fish species in aquaculture and experimentation are not providedwith such material since in vitro fertilisation is used. However, this possibly does not fulfilthe behavioural needs of the fishes if animals are highly motivated to build nests and leadsto frustration, stress and associated maladaptive behaviours. In other intensively farmedanimals such as pigs and chickens, providing females with nesting material had a dramaticimprovement on their behaviour and well-being (Cronin et al. 1998; Kruschwitz et al. 2008).Yet these materials are generally not provided to captive fishes even though they may have apositive impact upon behaviour and welfare. Indeed, the first recorded spawning behaviourof the round goby, Neogobius melanostomus, was observed in captivity by providing maleswith nesting material (Meunier et al. 2009). When nesting material was available, the malefishes spent a substantial amount of time engaged in nest building, courtship behaviour toattract females and parental care.

By applying knowledge of the natural behaviour of fishes, such as the requirement fornest building for reproduction to take place (Galhardo et al. 2009), significant improvementsto the captive environment can provide what fishes need to express their natural behaviouralrepertoire. This infers that welfare could be improved via a reduction in abnormal behaviourslinked to frustration from being unable to perform natural behaviours. However, to date therehave been no studies specifically examining this in fishes. Future studies should investigatewhether the welfare of captive species is enhanced by providing suitable substrates andmaterials necessary for mating to occur.

17.3.1.3 Diet

Dietary preferences are another way of ensuring that the appropriate nutrition and foodstuffis given to fishes. Fishes can be herbivores, carnivores or omnivorous (see Chapters 2 and 3);therefore, provision of the correct diet is vital if we accept that normal biological functioning

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equates to good welfare. Diet can affect behaviour and preferences in fishes; therefore,the animal’s hunger level must be accounted for when designing such experiments. In theintertidal fish, Girella laevifrons, food quality had a major impact on temperature preference.A highly nutritious diet resulted in these fishes selecting temperatures of 16◦C–18◦Cwhereas a lower quality diet resulted in fishes choosing lower temperatures of 10◦C–12◦C(Pulgar et al. 2003; Fig. 17.1c). These results were explained by optimisation of digestionand mechanisms of energy conservation in the low-quality diet treatment. In rainbow trout,the lack of vitamin C in the diet appears to lead to poor competitive ability and as suchthese fishes are mainly seen occupying the top layer of the aquarium tanks (Blom et al.1999). Supplementation of the diet with vitamin C resulted in these fishes occupyingthe preferred lower areas of the tank possibly through an increase in competitive status.When operating self-feeders, goldfish, Carassius auratus, were given the choice betweenthree diets differing in macronutrient composition (Sanchez-Vasquez et al. 1998). Goldfishactively chose the diet highest in carbohydrate and fat composition and selected against thehigh protein diet despite the fact that this may not be the ‘healthiest’ diet. These examplesillustrate how easy it is to determine dietary preferences in fishes and that improper dietcan cause significant shifts in behaviour. They also provide more evidence that fishes canmake choices by actively evaluating resources.

One area that has been neglected in studies of fish feeding is time spent foraging undernatural conditions versus how they are fed in captivity. If a particular species spends most ofits daily time budget foraging, does providing it with one or two feeds in a day in captivityresult in frustration? This has been observed in stabled horses which are fed monotonousfood stuff once to three times per day. In contrast, feral horses will spend up to 16 hours ina day foraging and individuals are highly motivated to perform this behaviour. Therefore,stabled horses exhibit signs of frustration and stereotypical behaviours, which can besignificantly reduced by altering the means and type of food provision. For example, hidingfood in different areas of the stable results in more time spent foraging accompanied by areduction in abnormal behaviour (Ninomiya et al. 2004). The motivation to forage for longperiods may have complicated effects on captive fishes but these have yet to be elucidated.Another factor to consider is whether live prey should be provided to predatory fish species.If individuals are highly motivated to hunt, then perhaps providing dead food is inadequate.Feeding of live invertebrates to fishes is generally considered acceptable and such food isavailable at most local pet shops; however, feeding of live vertebrates such as smaller fishis frowned upon. Research in large cats, such as tigers and servals, has shown improvedbehavioural indicators in captivity by providing these predators with hunting opportunitiesusing artificial prey (Markowitz & LaForse 1987). Future research should target thesequestions since they may provide evidence of how fishes are affected cognitively by thelack of feeding opportunities and as such how their welfare is compromised.

17.3.1.4 Social interactions

Fishes range from being territorial to highly gregarious; therefore, their preferences forbeing in close proximity with others or with related or unrelated individuals may varyaccording to the natural behaviour of a given species. The social context in which animalsare housed, as mentioned in Section 17.3, is vitally important since it can have a negative

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effect on fishes of low-social status in aggressive or territorial species when housed ingroups (Gilmour et al. 2005). Salmonid behaviour has received much attention since theyare a commercially important aquaculture and fisheries species. Holding salmonids in agroup results in the formation of a dominance hierarchy, where low-status fishes suffer acuteto chronic stress that can have deleterious effects upon growth and reproduction (Gilmouret al. 2005). In terms of biological function, this has a negative impact upon welfare, soholding this species in captivity can be problematic due to aggression (Conte 2004). Inthe natural situation, fishes are not confined to a relatively small area and can withdrawfrom aggressive interactions. Equally, holding gregarious species in isolation may resultin stress. Therefore, it is important to fully understand the social context of the naturalbehaviour of each fish species so that the correct decisions are made regarding stockingdensities, as well as the composition of group members. Again, this can be explored usingpreference tests.

In shoaling species, specific social preferences are known to exist where shoal composi-tion can be affected by relatedness, sex, age, dominance status, personality and phenotypeof polymorphic species (see Chapter 10). Therefore, it may be wise to better understand thenatural composition of shoals before placing fishes into groups in captivity to promote pos-itive welfare. For example, gender may have implications for the welfare of group memberswhere females are harassed by males for breeding as observed in guppies. This harassmentis believed to diminish female fitness via reduced foraging, augmenting predation risk,energy costs and disease transmission (Smith & Sargeant 2006). Therefore, female gup-pies may have better well-being when housed only with females. However, in the westernmosquitofish, Gambusia affinis, male harassment had no negative effects on female growthor fecundity but increasing the density of females whilst reducing male density had sig-nificant detrimental effects on female fitness (Smith & Sargent 2006). These contrastingresults from two closely related species highlight the important of species-specific require-ments. Therefore, future studies need to provide information on a variety of species to fullyunderstand how group composition affects welfare.

Theory predicts that shoals should be composed of similar individuals and that anyindividual that differs from the norm makes the shoal more conspicuous thereby increas-ing predation risk (Gomez-Laplaza 2009). Female Siamese fighting fish, Betta splendens,show significant preference for spending time near females rather than being in a cham-ber on their own (Blakeslee et al. 2009; Fig. 17.1d). These females also prefer to shoalwith similarly coloured females. However, placing females with males can result in highlevels of aggression and females are frequently killed by potential suitors. Such assor-tative shoaling has also investigated in juvenile angelfish, Pterophyllum scalare, whereindividuals of the uniformly black and golden colour morphs were held in groups with con-specifics of similar and dissimilar body colours to themselves, as well as in mixed-colourgroups. These fishes were given a binary choice to shoal with a group of conspecificscomposed of unfamiliar fishes of either a similar or dissimilar colour phenotype to them-selves. Fishes from the similar- and mixed-colour groups showed a significant preferencefor the similar shoal; however, those fishes in dissimilar groups showed no preference(Gomez-Laplaza 2009). Thus, previous experience affected assortative shoal choice and itis important to consider past housing history when interpreting the results of conspecificpreference tests.

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Captivity does present a rather different environment with contrasting selective pressures.For example, since there are no natural predators in laboratory situations, this strongselective force in nature has been removed and may affect the antipredator advantages toshoaling. In rainbowfish, Melanotonia duboulayi, captive individuals show no preferencefor familiar shoal neighbours yet wild population show a strong preference for familiarindividuals (Kydd & Brown 2009). This may reflect a relaxed approach to shoal compositionin captive fishes when predator threat is negligible. In contrast, wild populations may need tocreate tight cohesive shoals, which would be enhanced by forming shoals with fishes that arefamiliar with one another since each fish would know its place within the shoal. Therefore,when considering the results from captive-reared fishes, it is important to consider whethermotivational drivers have been removed under artificial conditions either via habituation orvia artificial selection. For example, providing food daily may reduce the need to expressforaging behaviour since the fish never experiences hunger or has to search over largedistances for food. This question needs to be fully explored by careful experimentation todetermine how captivity affects the well-being of fish and how it may impact upon theircognitive function.

Very few studies have explored whether conspecific choice in territorial fishes undercaptive conditions could be relevant to improving welfare. Some species have a preferencefor forming groups, breeding cooperatively or sharing refuges with related individualswhilst others selectively avoid kin (see Chapter 9). Brown trout, Salmo trutta, are naturallyterritorial fishes and show a strong preference for stream water containing no conspecificcues over that containing conspecific cues. When juveniles were given a choice betweenwater scented with siblings or non-siblings, the results were highly variable but mostindividuals showed kin avoidance (Ojanguran & Brana 1999). This may be adaptive interritorial species so that they do not compete with closely related individuals. In contrast,juvenile brook trout, Salvelinus fontinalis, show a strong preference for the odour of kincompared with non-kin in preference tests (Hiscock & Brown 2000). In Atlantic salmon,Salmo salar, kin preference was tested by holding pairs of related and unrelated individualswith either recirculating water to increase the concentration of chemicals cues involvedin kin recognition or a flow-through system where chemical cues were removed. Thepairs quickly formed a dominance relationship; however, water recirculation heightenedaggression, especially against unrelated fishes (Griffiths & Armstrong 2000). Therefore,water recirculation appears to have a negative impact on the welfare of the subordinatefishes if they are unrelated and, in this case, a flow-through system was beneficial inreducing aggression. Research into methods of reducing aggression in territorial species isnecessary to improve conditions for these species. Placing fish into novel, unfamiliar groupsmay promote aggression or stress; therefore, this should be considered when moving fishbetween aquaria.

17.4 What fishes do not want

Considering what an animal actively avoids is a useful way to understand what stimuli orexperiences a fish would seek to steer clear of. These must be important and, therefore, havenegative consequences for the individual. Fishes in classical conditioning experiments with

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negative reinforcement usually learn to avoid an aversive stimulus in a few trials or less (e.g.electric shock that may be painful, Ehrensing et al. 1982). Zebrafish can be trained to remainin a dark compartment of a shuttle box to avoid a weight dropping into the vicinity causingthe fish to display a startle response (Kim et al. 2009) and show avoidance behaviourat the sight of an animated predator (Gerlai et al. 2009). Fishes also show aversion tounpalatable food demonstrated by studies in the medaka, Oryzias latipes, where transgenicfishes with a lack of taste receptor genes fail to show aversion (Aihara et al. 2009). Manystudies have used electric shock as an aversive stimulus that would be painful to humans.Goldfish demonstrate a prolonged unwillingness to enter an area where they received ashock; however, when this area also contained food, eventually hungry fishes were willingto risk being shocked in order to eat (Millsopp & Laming 2008). Even though the fisheswere still given a shock in the area, they traded off the acute pain caused by the shock toget a resource that is crucial for survival. Therefore, these hungry goldfish were willing topay a cost in this case to gain access to a highly valued resource. The fishes may also havelearned that the shock is a very short stimulus and not life-threatening, and therefore, madethe decision based upon another important motivational state, hunger.

Studies on wild populations have provided many cases of fish avoiding certain stimuli,which may be used to discourage fishes from occupying areas where they are not wanted.In dams and reservoirs, where fishes are damaged in equipment that impairs their welfarebut also causes problems for humans, these avoidance approaches can be employed to deterfishes from being injured. Such an approach was used in a study on vendace, Coregonusalbula, where continuous artificial light was employed to prevent fishes from aggregat-ing (Schmidt et al. 2009). Vendace exhibited strong avoidance behaviour by swimmingdownwards when the light was turned on. With the careful deployment of artificial lightsthey stopped congregating in problem areas of the reservoir. Similar approaches are beingadopted where acoustic repellents are employed to prevent sharks getting entangled in netsand to prevent fishes entering power station coolant intakes (Maes et al. 2004). Thus, un-derstanding what fishes do not want or avoid can be a useful tool in the management andimproved welfare of natural populations. Avoiding such aversive stimuli as a managementapproach during captivity should also improve well-being. Welfare studies need to deter-mine what routine stimuli that fishes are exposed to in captivity (e.g. disturbance duringcleaning, vibration, excessive noise, etc.) would normally elicit an avoidance response anduse this information to develop better husbandry procedures. Behavioural observationsmade during these events could determine if there are any detrimental effects upon thefishes in terms of suspension of normal behaviour coupled with avoidance testing to obtainan insight into whether these experiences are aversive to the fishes.

17.5 Pain and fear in fish

The key question in negative emotional states is whether fishes consciously experiencethem. Do fishes suffer when damaged? Does a fearful situation result in mental sufferingin fishes? These are difficult questions since they require knowledge of how fishes feel.Since we cannot tell what another human is feeling unless they communicate it to us, howare we supposed to know how an animal feels? Rather than addressing these questions

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directly, behavioural observations and cognitive approaches have been adopted to under-stand how significant these negative affective states are to the animal. In other words,fishes can give us some indication of how they feel by altering their behaviour in somequantifiable way. So far, it has been demonstrated that teleost fishes possess nociceptors,receptors that preferentially detect painful stimuli; have pathways from the periphery tothe brain; the brain is active during painful stimuli; the fishes display adverse changes inbehaviour and physiology indicative of suffering that are ameliorated by morphine; andcan learn to avoid painful events like electric shock and hooking usually in one trial (re-views in Sneddon 2004, 2006, 2009; Chapters 15 and 16). Possible anticipation and learnedavoidance of painful events may demonstrate that fishes will react strongly to evade thesebehaviours or stimuli that will result in an aversive or painful state. This suggests somelevel of consciousness in fish since the fish must have such a strong negative experienceassociated with these events that they are motivated to avoid them often after one exposure.One can prove that fish can detect, react and show complicated, prolonged behaviouralchanges that are not simple reflexes, but are these indicative of how important pain isto them.

Using selective attention strategies based upon the idea that individuals have a limitedpool or capacity to their attention may provide a means of gauging the significance of pain.If the fish’s attention cannot be diverted away from pain-related responses to apparentlyimportant competing stimuli, then pain is more important. When given a pain stimulus,rainbow trout did not show an appropriate fear response to novel object testing whereascontrols exhibited a significant neophobia. Administering morphine resulted in pain-treatedfishes returning to a normal neophobic response (Sneddon et al. 2003b). This suggests thatpain was dominant over fear with respect to the attention of the fish. Similarly, when fishesexperiencing pain were given a predator cue, they did not show the typical antipredatorresponses that the controls performed, i.e. increased escape attempts and increased refugeuse (Ashley et al. 2009; Fig. 17.2a). Again, pain takes priority over diverting attention topredation, which would be detrimental in a natural context. Interestingly, dominant trout in

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Fig. 17.2 (a) The mean percentage change in refuge use and escape behaviour in rainbow trout that were injectedsubcutaneously with saline as a control or acetic acid. (b) The mean frequency of aggressive chases performedby dominant rainbow trout before (normal) and after (Treatment) injection with saline and placed into a familiar(CF) or unfamiliar (CU) social group or injected with acid. (AF, familiar; AU, unfamiliar; **P < 0.001.) (Modifiedfrom Ashley et al. 2009. Copyright 2009, with permission from Elsevier.)

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social groups exhibited none of the physiological signs of pain (enhanced ventilation rate,increased cortisol), but when returned to their familiar group they decreased the amount ofaggression over three hours. By contrast, when dominants were returned to a novel group,no suspension in aggressive behaviour was seen whilst they were in pain (Ashley et al.2009; Fig. 17.2b). Given the importance of dominance status in trout which governs accessto resources and results in enhanced fitness, it would seem exerting dominance is moreimportant than exhibiting signs of pain. Studies on birds and mammals have demonstratedthat they do not show signs of pain in novel situations or when conspecifics are presentand this has been interpreted as the animals being motivated to avoid showing signs ofweakness in a risky situation (Gentle 2001; Arras et al. 2007). Therefore, in the troutstudy, it may be that the presence of unfamiliar conspecifics results in noxiously treatedtrout refraining from exhibiting any signs of pain in order to maintain their social status.Together, the trout studies confirm that the trout’s behavioural responses to pain are indica-tive of some form of discomfort and suffering and are not the simple reflex responses thatcritics claim.

Species-specific differences have been identified where trout and zebrafish show anelevated ventilation rate and reduced activity in response to a standard pain test, but commoncarp do not. Carp and trout show anomalous behaviours such as rubbing the affected siteand rocking from either pectoral fin (similar to fishes attempting to maintain an uprightposition); however, zebrafish do not (Reilly et al. 2008). Collectively, these studies indicatethat rather than being only able to show stimulus-response behaviour, different species offishes are capable of prolonged, complex responses suggesting that they experience thenegative affective component of pain which is distracting enough to prevent them fromperforming other behaviours.

Emotional conditioning using fear paradigms are well documented in fishes (see Chapter13). Fear behaviours such as the startle response, freezing, escape and so on can easilybe measured. Very few of these studies have been applied to an animal welfare contextor have explored the negative feelings associated with fear. Fear responses in rainbowtrout have been investigated using classical conditioning with negative reinforcement (Yueet al. 2004). Here, fish associated a light cue with an aversive chase by a plunging net.After training, fish responded to the light cue before net presentation by swimming toanother compartment to avoid being chased. This experience was significant to the fishsince memory recall was demonstrated after seven days. Other studies have demonstratedescape responses lasting for approximately 11 months in rainbowfish (Brown 2001). Usingthis approach it may be possible to quantify the motivation of the fish to avoid a fear-causing stimuli by using the length of memory recall to gauge how important the eventwas. Caution has to be used here since it has been suggested that true decision-makingprocesses or very high-level cognitive processes are not involved in classical conditioning(Rose 2002). However, subsequent behaviour is affected by these training paradigms. Iffishes are able to anticipate negative events and produce a response prior to it occurring,then this is evidence of cognitive processing rather than a reflex response. Experimentsusing classical conditioning between an aversive stimulus and a neutral cue should bedesigned to carefully differentiate between those behaviours motivated by the animal’saffective state or higher cognitive functions rather than the stimulus response processes ofassociative learning.

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17.6 Personality in fish

Personality is often applied to humans; however, the philosophical and psychological def-inition is the possession of traits that characterise one individual from another (Eysenck1946) and can readily by applied to fishes (Chapter 7). One of the most commonly studiedaxes of fish personality is the shyness–boldness continuum. Boldness can be measured asthe willingness to take risks when encountering a novel challenge (e.g. Frost et al. 2007).These divergent phenotypes also exist in natural populations. Brook charr collected fromthe wild continued to exhibit bold and shy personalities in the laboratory with bold fishesperforming more exploration and activity in a novel environment. However, in response toa fear test, a uniform startle response was observed that was independent of personalitytype (Wilson & McLaughlin 2007). Therefore, the responses to threatening stimuli wasnot linked to personality in this species. However, in studies on pain bold fishes appear torecover more quickly compared with shy fishes and in the antipredator experiments boldfishes experiencing pain actually decreased their use of refuges after a predator cue waspresented which is contrary to the responses of control fishes (Ashley et al. 2009). Whetherthis demonstrates a real difference in cognitive processing between the two phenotypes oris reflective of how they cope with stress is yet to be established.

Behavioural needs can be considered as those resources in an animal’s environment thatallow the expression of a normal behavioural repertoire (Jensen & Toates 1993). In termsof behavioural needs and welfare, bold fishes may have different requirements to shy fishes,especially in species where boldness correlates with aggression. In captive experimentsbold trout generally dominate shy trout (Frost et al. 2007); therefore, shy fishes are likely tobecome stressed if overt aggression is continually used by bold, dominant fishes (Gilmouret al. 2005). Since faster growing fishes have been selected for in aquaculture, this strategyhas co-selected bold, aggressive fishes which can present problems for any subordinatesin terms of chronic stress (Huntingford 2004). This difference in dominance status alsoaffects captive fish behaviour and use of substrate in the Mozambique tilapia, Oreochromismossambicus, where dominant males preferred a soft substrate as opposed to no substratebut subordinate males did not show such a preference (Galhardo et al. 2009). Dominantmales are likely to secure matings and use the substrate as nesting sites; therefore, theprovision of a substrate may have positive implications for breeding male welfare. Fishesdo have the capacity to modulate their behaviour and make an adaptive response in differentcontexts, which is suggestive of higher cognition – the ability to make decision dependentupon an evaluation of external factors (Chapter 7).

17.7 Wider implications for the use of fish

Considering the evidence for cognitive ability and awareness in fishes, for their capacity torespond to and learn to avoid negative events such as pain and fear, and for their ability tochoose between resources so that clear preferences can be identified, this suggests that fishesshould be considered capable of experiencing poor welfare states and that these should beminimised. Even if some doubts remain which may be waylaid by future research, theprecautionary principle should be adopted as best practice.

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Fishes are subject to practices that would be unacceptable in other vertebrates, yet manymore individuals are harvested in aquaculture, recreational and commercial fisheries thanin production for terrestrial meat, poultry and dairy products. Fishes are also subject toinvasive procedures in scientific experimentation although there are regulations protectingtheir use including humane guidelines in most countries. Finally, fish can be purchasedas a companion animal by members of the public who may have no experience in fishhusbandry. These issues are discussed in the following sections with reference to fishwelfare and cognition.

17.7.1 Aquaculture

Many practices associated with aquaculture such as high stocking density, transportationin confined vessels and tanks, food withdrawal prior to slaughter and slaughter itself alsoresult in stress and are considered problematic from a welfare perspective (Ashley 2007;Table 17.1). Farmed fishes are generally held in a very simple, monotonous environment inhigh densities (Chapter 16). They are not provided with the opportunity to select their habi-tat, food, mates or perform their normal behavioural repertoire such as nest building. Highstocking density can lead to high transmission of diseases that are necrotic and cause tissuedamage that may be painful. All of these factors are known to lead to abnormal behaviours,such as functionless, repetitive stereotypies, in farmed and captive mammals (Jensen 2009).Yet relatively little information is available as to whether fishes are detrimentally affectedby many of these procedures. Questions regarding the cognitive functioning of farmedfishes are rare so future studies should tackle the impact of aquaculture procedures uponthe behaviour and welfare of these fishes.

Farmed fishes are also subject to unpredictable, stressful disturbances such as vacci-nation, size grading, cleaning and movement between tanks (Conte 2004; Ashley 2007).These are likely to impair welfare and increased stress or mortality has been recordedafter these events. This also results in frequent changes in social composition within thetank environment. The impact of being unable to associate with preferred or familiar in-dividuals in captivity needs to be investigated since high stocking density reduces normaldominance hierarchy formation. This could result in increased aggression when fishes arecompeting for dominance status as seen in pig farming. Mixing of unfamiliar pigs resultsin substantial overt aggression and injuries. Simple practices such as providing ad libitumfood to reduce competition (Barnett et al. 1994) and mixing pigs of different sizes and thusaggressiveness substantially reduce these problems (Erhard et al. 1997). To resolve theseissues of subjecting fish to uncontrollable and unpredictable stressful events, stimuli couldbe introduced to indicate when aversive stimuli are about to occur. For example, a toneor light could turn on to pre-empt common procedures such as cleaning. If these eventsare more predictable, it enables fishes to prepare themselves for the impending event andmay reduce stress levels. Other strategies, such as using an avoidance response to facilitatefishes to move of their own accord, have been successful. Trout avoid carbon dioxide asdemonstrated by a fish farm based study where increased dissolved carbon dioxide levelsresulted in fish swimming through a pipe to the neighbouring tanks (Clingerman et al.2007). This approach was extremely successful and avoided any mechanical disturbance orair emersion thereby improving welfare.

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Table 17.1 The major welfare issues fish experience in aquaculture and suggested improvements.

Area of welfare concern Welfare issues involved Improvements

Winter diseasesSeveral diseases associatedwith low temperatures

Although many are clearly associatedwith specific bacterial pathogens,immunosuppression during wintermay play a large role.

Immunisation

Adapted diet providing asupplementary dosage of vitaminsand trace minerals to assist theimmune system and altered feedingregime controlling level of nutrientsavailable to the pathogen.

Fin rotAbrasion with theenvironment and/oraggressive interactionscause fin damage andsecondary infection mayfollow

Injectable vaccines have supersededantibiotics although vaccines andadjuvants are associated withinflammation and granuloma, as wellas the stress of handling anaesthesiaand injection.

Vaccines with improved efficacy andreduced side effects as well as oralapplication.

Sea liceParasitic copepods maycause severe tissue damage

Lice have developed resistance totraditional chemical treatments.

Potential alternative controls includevaccination and selective breedingtowards louse resistance

Biological control with cleanerwrasse but should consider wrassewelfare.

Viral diseasesExamples: Infectiouspancreatic necrosis,infectious haematopoieticnecrosis, viralhaemorrhagic septicaemia,infectious salmon anaemia,sleeping disease

Traditional vaccines developed overthe past 20 years have shown onlymoderate success and there arerelatively few commercial vaccinesand specific therapeutics withadequate efficacy.

The development of alternativeanti-viral treatments such as DNAvaccines and selection for diseaseresistance.

Non-infectious production-related deformitiesDeformities of the heart,swim bladder and spine

Fish with heart deformities show ahigh mortality rate during stress dueto impaired cardiovascular function,cardiac failure or heart rupture. Bothgenetic and environmental factorsmay contribute to spinal deformities.

High temperatures during incubationof salmon should be avoided. Spinaldeformities may be reduced byincreasing smolt weight at seawaterintroduction, vaccinating andreducing salinity and temperaturevariations. Fish from familiesshowing a high incidence ofdeformities should not be used forbreeding.

Grading, handling and crowdingInherently stressful Many procedures, such as grading,

are aimed at improving welfare.There is a large variation betweenspecies in stress response toprocedures and handling stressorscan affect subsequent stress response.

Appropriate supplementation ofdietary vitamins C + E and glucanmay protect against the adverseeffects of chronic stress.

The appropriate use of good crowdmanagement, suitable nets, carefulhandling, recovery periods andmovement using fish pumps andtransfer pipes is preferable.

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Table 17.1 (Continued)

Area of welfare concern Welfare issues involved Improvements

Appropriate feeding techniqueand stocking densities may avoidfrequent grading.

TransportationInherently stressful as it mayinvolve capture, loading,transport, unloading and stocking

Transport stressors can affect fishover a prolonged period.

Adverse effects may be reducedby suitable acclimation andrecovery periods as well as speciesappropriate use of anaesthesia anddilute salt solutions.

Food withdrawalStarvation prior to slaughter,transportation and othermanagement practices

May benefit welfare by reducingmetabolism, oxygen demand andwaste production. AlthoughAtlantic salmon and rainbow troutshow long anorexic periods in thewild so the welfare effect of fooddeprivation in aquaculture is notknown. Deprivation for shortperiods under appropriateconditions may not diminishwelfare.

Starvation for up to 72 h forAtlantic salmon and 48 h forrainbow trout should only occurwhere beneficial to welfare andempirical studies on the effects ofstarvation on stress physiology orbehaviour are required.

SlaughterSlaughter should be as humane aspossible – fish should be stunnedprior to slaughter, causing animmediate loss of consciousnessthat lasts until death

Dewatering followed byasphyxiation in ice slurry ofrainbow trout and gilt head seabream; immersion in CO2

saturated water followed by gillcut or gill cutting alone forAtlantic salmon and rainbowtrout; and de-sliming followed byevisceration of eels do not meetthe criteria for humane slaughter.

Percussive or electrical stunningmethods appear to achievehumane slaughter in Atlanticsalmon, gilt-head sea bream,turbot, and rainbow trout.

The use of electric stunningtongues or electrically stunningbatches of eels in freshwatercombined with nitrogen flushingcan cause immediateunconsciousness.

Stocking densityPivotal factor affecting welfare ina number of different ways (e.g.through aggression, water quality,and activity/feeding patterns)

The effect of stocking densitycomprises of numerousinteracting and case-specificfactors. Sea bass show high stresslevels at high densities. Arcticcharr show low growth and foodintake at low and very highdensities. Halibut tolerance forhigh-stocking density appears tobe stage dependent. Rainbowtrout show a decrease in welfare athigh densities, water quality beinga key factor. High-stockingdensities, above a given threshold,are associated with reducedwelfare in Atlantic salmon in seacages. Site-specific factors alsohave an effect on welfare.

Feeding pattern and floor spacemay be altered to improve theeffect of density on welfare inhalibut, also see ‘Aggression’.

Salmon-swimming depth andshoal density can be manipulatedby artificial light levels, andfeeding patterns can alteraggressive interactions in severalspecies including Atlantic salmon.

(continued)

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Table 17.1 (Continued)

Area of welfare concern Welfare issues involved Improvements

AggressionFormation of social hierarchiesmay lead to injuries, chronicsocial stress and sizeheterogeneity

Sociobiology, stocking densityand feeding technique have stronginfluences on the levels of socialinteractions.

Feeding technique should bespecies appropriate to avoidexcess competition andaggression.

The presence of a small number oflarger fish may reduce aggressionwithin groups of smaller fish.

Increased dietary levels ofl-tryptophan has been shown tosuppress aggressive activity.

Substrate or background colourmay be used to influenceaggressive behaviour in somespecies.

Abnormal behaviour and thefreedom to express normalbehaviour

Abnormal behaviour includesrepetitive behaviour and abnormalswimming activity/patterns

Understanding the functionalorigin of apparently abnormalbehaviour is important. Empiricalstudies are required to establishwhether abnormal behavioursrepresent diminished welfare oradaptive responses with no effecton welfare.

Enriched rearing environmentsmay improve welfare followingrelease to augment wildpopulations.

Without empirical studies theimportance of a given behaviouralpattern to a given species isunclear. Studies of the mechanismof control and/or the behaviouraland physiological consequencesof denial of expression of keybehaviours are required.

Choice studies may allowassessment of the value associatedwith a given behaviour orresource.

Source: Adapted from Ashley (2007), with permission from Elsevier.

When harvesting, fishes are crowded into a small area and become observably stressed,showing flanks and have increased cortisol concentrations. This can be ameliorated bymoving farm sea cages to a much lower depth reducing light levels and catching and killingthe fishes more quickly (Brown et al. 2010). Reduced stress in the fishes during harvest notonly has ethical benefits but may also improve the quality of the fillet thereby increasingeconomic return (e.g. Bahuaud et al. 2010).

Aquaculture has also promoted the selection for fast growth by breeding the quickestgrowing individuals and producing bolder, more aggressive fishes (Sundstrom et al. 2004).As personality traits affect survivorship, this has resulted in farmed fishes released forrestocking purposes outcompeting wild populations due to their aggressiveness (Sundstromet al. 2003), but has made these bold fishes more vulnerable to predators (Chapter 16). This

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raises questions as to whether it is ethically sound to use farmed fishes that have noexperience of spatially complex environments or how to react to predators for restockingdepleted rivers and lakes (Brown & Day 2002). If they are inept at surviving in the naturalenvironment and have a detrimental effect on wild populations, it would seem ineffectiveand morally corrupt to use them in this way. Studies have explored the possibility ofameliorating these effects by teaching farmed fish antipredator and foraging skills prior torelease to enhance their survivorship (Chapter 16; Brown & Laland 2001). This providesan excellent example as to how cognitive approaches can play important roles in appliedmanagement contexts and should be further explored in future studies.

Altogether, one may consider the welfare of farmed fishes not to be ideal but fishes doprovide an important source of protein. The aquaculture industry has attempted to under-stand and improve the well-being of fish (Table 17.1). However, implementing changes suchas reduced stocking density is likely to enhance the costs of production similar to that seenin free range, welfare-friendly meat where the increase in price can be considerable. Con-sumers should demand to know where the fish they buy came from, under what conditionsthey were kept and how they were caught to make ethically based decisions.

17.7.2 Fisheries

Large-scale fisheries also employ procedures that are likely to impair the welfare of caughtfishes (Chapter 16). Trawling, dredging, hooking on long line, and capture in nets (e.g.cast, drift, ghost, gill, seine) are known to cause stress and under some conditions mortality(Turunen et al. 1994; Chopin & Arimoto 1995; Metcalfe 2009). Fishes are usually hauledout of the water causing suffocation, deposited on deck or within the vessel and killed by avariety of means including suffocation on ice (Ashley 2007). If fishes have the capacity toexperience some form of pain and fear, we must consider this unacceptable. Live chillingresults in increased physiological stress (Lambooij et al. 2002) and suffocation on icecan take up to 200 minutes for brain death to occur (Robb & Kestin 2002). Humanekilling should be quick and effective and although percussive stunning which causes braindestruction could be used as seen in fish farming (Roth et al. 2007), this may be impracticalfor the enormous numbers of fish caught in large-scale fisheries. Much research remainsto be conducted to improve fisheries practices and to understand whether these do indeedimpair welfare, cause suffering and to what extent. Many fishes that are caught are non-targetspecies and are considered a by-catch, which are discarded. Studies aimed at understandingwhether these fishes have impaired welfare as a consequence of being caught are necessarysince some species suffer 50% mortality as a result of the capture process (Mandelman &Farrington 2007).

17.7.3 Recreational fishing

In many respects recreational fishing is similar to any other form of hunting but fishingdoes not receive the same sort of social stigmatism or raise as much objection because fishare not perceived in the same way as other animals. Recreational fisheries or angling forsport is often conducted purely for enjoyment and may involve catch and release of fishes.Fishes are hooked, landed and then released and are known to suffer stress (Arlinghaus et al.

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2007, 2009) and impaired behaviour post-release (e.g. Cooke & Philipp 2004; Danylchuket al. 2007). This is in contrast to catch and kill where fishes are killed presumably to beeaten by the angler. However, lengthy capture causes stress and fish should not be allowed tosuffocate in air since this takes approximately 15 minutes for death to occur in trout (Robb &Kestin 2002). Given that the catch and release of fish may result in injury from hooking,exhaustion, air emersion, stress, removal from their natural environment and mortality,then the fish’s welfare is clearly compromised. Damage to the fish during hooking and netabrasion when landed (Butcher et al. 2008) are likely to be painful events and result in astress ‘fight or flight’ response, producing fear and/or negative states associated with stress.

One can accept there is a benefit to humans when fishes are humanely killed for foodso long as the fish is killed rapidly after capture; however, the question of practising catchand release must be considered from a moral and ethical perspective. Fishes are ableto learn to avoid hooks after being caught and released (Ferno & Huse 1983; Pyanov1993; Young & Haye 2004; Chapter 16); therefore, this aversive stimulus has a significanteffect upon subsequent fish behaviour. Many angling organisations and scientists havemade recommendations for improved catch-and-release practices to improve the welfareof caught fish (Schupplid 1999; Freshwater anglers, Australia in; Cooke & Sneddon 2007;Table 17.2). Such practices include the use of barbless hooks and knotless nets. Germanyhas responded to this moral question by restricting the capture of fish for food purposesonly (Arlinghaus & Mehner 2003). However, more research is needed to fully understandhow catch-and-release practices affect the fish in both the long and short terms.

17.7.4 Research

Unlike many other realms where fishes are widely used, the use of fish in research is heavilycontrolled by legislation in most developed nations. Nevertheless some issues remain.Experimentation of fish does involve maintaining large numbers in captivity. This is oftenconducted using barren stock tanks. Since fishes have specific preferences for substrate,refuge, nesting material, related individuals and so on, environmental enrichment should

Table 17.2 The main recommendations made to anglers to improve welfare to the fish in recreational fishing.

Welfare concern Welfare issues Improvement

Exhaustion and stress duringlong angling event

Stress, fear and prolongedrecovery impairing subsequentbehaviour

Minimise the duration of theangling event; reduce play time

Air emersion and handling Stress, suffocation and damageduring handling

Minimise or eliminatehandling and exposure to airby keeping fish in water

High water temperaturesassociated with increasedstress and mortality

Stress and prolonged recoveryimpairing subsequentbehaviour or death

Restrictions in angling athigher water temperatures

Damage caused by hookingcan result in injury or mortality

Pain, fear, stress or death Using hooks that reduce injury,stress or mortality

Impaired reproductive success Stress affects reproductivecapacity

Avoid angling duringreproductive period

Source: Adapted from Arlinghaus et al. (2007) and Cooke & Sneddon (2007), with permission from Elsevier.

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be explored as a means of improving welfare. This would obviously need to be specific tothe species requirements.

Moving fishes between tanks should also be carefully considered since if fishes prefer toshoal or hide with familiar individuals, placing them in new groups or in novel environmentsis likely to be stressful. Aggressive species which form dominance hierarchies may needto be held in high numbers to reduce such behaviour so group composition and density arealso important factors. If fishes rely upon information transfer and learn from conspecifics,then if one fish within a tank is stressed and acting abnormally then surely this will affectall fishes within the tank. Future studies should address these welfare concerns within therealm of the laboratory aquaria by using cognitive approaches such as preference testing.Comprehensive knowledge of the life history and normal behaviour of each species is vitalto understand how captive conditions may impair fish behaviour.

17.7.5 Companion fish

Finally, our use of fish as pets should be highly scrutinised given their increasing popularity.Part of the problem stems from the very low cost of purchasing fish as a pet and the ease ofavailability. Fortunately, in most countries, goldfish in a plastic bag can no longer be offeredas a fairground prize. The classic image of a solitary goldfish in a barren, small goldfishbowl seems unreasonable given the complicated nature of fish behaviour and preferencesfor social and environmental stimulations. It is also believed that due to a low surface areathey provide insufficient dissolved oxygen for fish to breath and indeed these sphericalbowls have been banned in Rome, Italy. No licensing or training is required to set up anaquarium tank and keep fish, yet it is clear that an understanding of these aquatic animalsis necessary to maintain them in good health. This is in stark contrast to the situation withmost other pets where, in many countries, owners of cats, dogs and reptiles need to beregistered.

Another aspect of the ornamental fish trade is identifying where the fishes have comefrom. Some fishes are bred in captivity specifically for the pet trade but many are takenfrom the wild depleting natural populations. They are frequently harvested in unsustainableways, for example the use of clove oil to stun entire populations on coral reef bombies.These fishes are placed into plastic bags containing aerated water but can be transportedfor extended periods of time without further aeration and with deteriorating water quality(Walster 2008; IATA 2009). In guppies, post-transport mortality is linked to high stresslevels (Lim et al. 2003). Research aimed at understanding and improving the procedures inthe ornamental fish trade is necessary since currently relatively little is known about whatspecific welfare problems exist.

17.8 Conclusion

Cognitive experimental approaches are extremely useful in understanding the subjectivestate of fish and determining how negative welfare states impact upon fish behaviour. Weuse fishes in a variety of ways subjecting them to practices that would not be consideredacceptable in other vertebrates. Therefore, careful consideration of fish behaviour, physi-ological functioning and welfare are needed. Preference testing can inform husbandry of

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428 Fish Cognition and Behavior

captive fish since if fish actively choose specific items such as shelter or substrates then theymust be beneficial in terms of what options were given. Avoidance tests employing aversivelearning paradigms can also deliver important information on what fishes find harmfuland can also be informative for fish husbandry. Housing conditions in captive fish havereceived attention from regulatory bodies with environmental enrichment now considerednecessary in the laboratory aquarium (e.g. Europe, Sauer 2004). However, it is vital thatspecies-specific requirements are developed since what one fish species prefers anothermay not and this could be detrimental to welfare.

Environmental enrichment is known to promote brain development in fishes (Lemaet al. 2005; Kihslinger et al. 2006) and may stimulate learning ability (Brown et al. 2003;Salvanes et al. 2007). Providing habitat complexity may be a valuable tool for improvingwelfare of captive fishes. Rearing fishes in isolation can also affect brain size (Gondaet al. 2009); therefore, social housing may have stimulatory effects directly upon braindevelopment, which has consequences for behaviour and possibly welfare. More researchis needed on social and environmental enrichment to make reliable and valid conclusions.

Negative emotional states such as pain and fear do result in profound changes in be-haviour and physiology. Pain may prevent animals showing normal fear and antipredatorresponses; however, the context is very important and one must consider species-specificdifferences. Studies on fear and pain should be designed to allow animals to make a choiceto avoid these states but more advanced paradigms other than classical conditioning couldbe used to truly understand the cognitive implications of these negative states. Studies di-rectly tackling higher cognitive functions such as self-recognition should be designed withthe biology of fishes in mind rather than applying paradigms from mammals. Fishes rely ondifferent sensory systems and may recognise themselves through smell rather than throughvision in mirror tests. If higher cognitive abilities are identified in fishes, this would makea real advance in our understanding of whether fishes are conscious of pain and fear and asa consequence suffer.

Assessment of negative welfare may be confounded by individual differences wherebold fishes recover more quickly from stressful events. Housing conditions may promotewelfare in bold fishes but as a consequence may be detrimental to shy fishes where they aredominated by bold individuals. Cognitive approaches should be developed to understandwhether differences in learning ability are due to underlying mental processes or are simplya result of the risk-taking bold phenotype being more willing or motivated to engage inlearning trials (Roult et al. unpublished data).

Finally, the question of whether captive conditions remove certain motivationally drivenbehaviour is an important one. Does regular feeding of caged Atlantic salmon in aquacultureremove the need for these fishes to travel long distances to find food as they would do innatural populations? Or do the fishes swim continuously in a circular fashion to expressthis behaviour in the confines of the sea cage? Does the absence of predators in laboratoryaquaria result in reduced or absent antipredator behaviours in captive fish populations andsubsequently their fear concepts? These and many other questions should be addressed infuture cognitive experiments where comparisons with the natural behavioural repertoireof the wild counterpart will provide insight into the behaviour and welfare of captivehoused fishes. Only then can we really understand how our use of fishes impacts upon theirwell-being.

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Acknowledgements

I am grateful to Culum Brown and two anonymous referees for their useful comments onthis chapter. I wish to thank NERC, The Leverhulme Trust and UFAW for funding.

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