Simon Mackenzie

Arjan Palstra

Josep Planas

David J Mckenzie
email: david.mckenzie@cnrs.fr

Marie-Laure Bégout

Helgi Thorarensen

Marc Vandeputte

Daan Mes

Sonia Rey

Gudrun De Boeck

M.-L Bégout

P Domenici

P V Skov

Aerobic swimming in intensive finfish aquaculture: applications for production, mitigation and selection

ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

Introduction

The aquaculture research community is interested in the potential applications of swimming exercise as a tool to promote the productivity and welfare of some intensively farmed fish species. This interest crystallized as an EU COST Action (FA1304 Fitfish) that provided a forum to discuss the potential uses of exercise in finfish aquaculture. A critical reappraisal of the literature is now timely [START_REF] Palstra | Swimming physiology of fish: Towards using exercise to farm a fit fish in sustainable aquaculture[END_REF], so this review provides a concise analysis of current knowledge focussing on three major applications for swimming, namely production, mitigation and selection.

With regard to production, sustained aerobic exercise has been reported to stimulate growth and/or improve feed conversion for a variety of farmed species, under experimental conditions [START_REF] Davison | Swimming-Enhanced Growth[END_REF]. This is of obvious potential interest, we review the latest evidence and the potential underlying mechanisms, which range from animal behaviour (Jørgensen and Jobling, 1993;[START_REF] Skov | Effects of rearing density and water current on the respiratory physiology and haematology in rainbow trout, Oncorhynchus mykiss at high temperature[END_REF] to muscle cell biology [START_REF] Ibarz | Sustained swimming improves muscle growth and cellularity in gilthead sea bream[END_REF]. In terms of mitigating the deleterious impacts of intensive aquaculture on the welfare of fishes, exercise has been reported to alleviate chronic stress [START_REF] Young | Effects of Exercise Conditioning on Stress Responses and Recovery in Cultured and Wild Young-of-the-Year Striped Bass, Morone saxatilis[END_REF] and to promote recovery from acute stresses [START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF][START_REF] Milligan | Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout[END_REF]. It may also improve disease resistance [START_REF] Castro | Aerobic training stimulates growth and promotes disease resistance in Atlantic salmon (Salmo salar)[END_REF], promote neuroplasticity and cognition [START_REF] Mes | Swimming exercise enhances brain plasticity in fish[END_REF], and inhibit precocious sexual maturation [START_REF] Graziano | Swimming exercise to control precocious maturation in male seabass (Dicentrarchus labrax)[END_REF]Palstra et al., 2010a). We review the evidence for these positive effects and their underlying mechanisms.

We briefly consider how observation of swimming behaviour may provide 'operational welfare indicators' (OWI), especially in early life stages.

In terms of using exercise as a tool for selection, this could have various applications.

Exercise tests may be useful in identifying robust animals within a population that are best suited for grow out, for example for transfer to sea pens, and may be able to distinguish fish for their stress coping styles. Exercise tests could also be used for trans-generational selection of robust families, so we review the evidence that exercise performance is a heritable trait in fishes [START_REF] Vandeputte | Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax)[END_REF].

Exercise and production: effects on growth

Studies on the effects of exercise training on growth in fishes arose initially to resolve the question of whether fish muscle displayed the same degree of plasticity as their mammalian counterparts, when subjected to an exercise regime [START_REF] Davison | Training and its effects on teleost fish[END_REF]. Several parallel fields of fundamental research examined how swimming exercise (and 'training') might affect variables such as muscle fibre sizes and densities [START_REF] Davison | The effect of prolonged exercise on the lateral musculature of the brown trout (Salmo trutta)[END_REF][START_REF] Rasmussen | Moderate exercise of rainbow trout induces only minor differences in fatty acid profile, texture, white muscle fibres and proximate chemical composition of fillets[END_REF], overall exercise performance capacity [START_REF] Gallaugher | Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming[END_REF], and the use of metabolic fuels [START_REF] Alsop | The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss)[END_REF][START_REF] Richards | Substrate utilization during graded aerobic exercise in rainbow trout[END_REF]. There was also a research focus upon a more applied aspect, namely whether aerobic exercise could be used to improve growth rates when farming fish species that, in nature, have an active lifestyle. This subject has been extensively reviewed [START_REF] Davison | The Effects of Exercise Training on Teleost Fish[END_REF][START_REF] Davison | Training and its effects on teleost fish[END_REF][START_REF] Davison | Swimming-Enhanced Growth[END_REF]Jobling et al., 1993) but new approaches and species continue to accrue, demanding a consideration of current status and future directions. Although it is frequently reported that fishes submitted to moderate swimming exercise have higher growth rates than those held in still water or at low currents (e.g. [START_REF] Ibarz | Sustained swimming improves muscle growth and cellularity in gilthead sea bream[END_REF][START_REF] Palstra | Forced sustained swimming exercise at optimal speed enhances growth of juvenile yellowtail kingfish (Seriola lalandi)[END_REF][START_REF] Shrivastava | Exercise improves growth, alters physiological performance and gene expression in common carp (Cyprinus carpio)[END_REF], other studies have found that swimming exercise has no, or even negative, effects on growth (e.g. [START_REF] Kiessling | Influence of Sustained Exercise at Two Ration Levels on Growth and Thyroid Function of All-Female Chinook Salmon ( Oncorhynchus tshawytscha ) in Seawater[END_REF][START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF][START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF].

Growth and energy balance

At its most basic definition, growth is an increase in body mass due to consumption of food [START_REF] Jobling | Environmental Factors and Rates of Development and Growth[END_REF]. In principle, growth of fishes (Fig. 1) depends on the balance between the energy assimilated from consumed food and the amount of that energy dissipated for metabolism, the 'costs of living'. These metabolic costs comprise (1) standard metabolic rate (SMR), the cost of basal organismal maintenance; (2) specific dynamic action (SDA), the costs of nutrient digestion, assimilation and tissue deposition, and (3) the costs of routine activities such as swimming, immune responses and reproduction. The remainder of the assimilated energy equals the theoretical net gain and 'growth' of the fish, although this is also influenced by the efficiency with which nutrients are converted to energy or tissue accretion [START_REF] Brett | Scope for Metabolism and Growth of Sockeye Salmon, Oncorhynchus nerka , and Some Related Energetics[END_REF][START_REF] Brett | Physiological Energetics[END_REF][START_REF] Jobling | Environmental Factors and Rates of Development and Growth[END_REF][START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF].

An increased growth rate in fishes subjected to swimming exercise is commonly referred to as 'improved', 'optimised' or 'enhanced'. It is essential, however, to distinguish whether an increased growth rate is simply due increased feed consumption, as opposed to increased retention of energy and nutrients. That is, from a perspective of the profitability and environmental impact of aquaculture, 'exercise-enhanced growth' is really only promising if it is associated with improved efficiency of how food energy is retained as body mass, namely an improved feed conversion ratio (FCR) and/or an improved retention of dietary protein.

Energetic costs of aerobic swimming

Aerobic swimming is muscular work so it of course has an energetic cost, which is typically measured indirectly as rates of oxygen uptake when fish are obliged to swim at set speeds in a swim-tunnel respirometer (Brett, 1964;[START_REF] Webb | Swimming[END_REF][START_REF] Mckenzie | Swimming and other activities | Energetics of Fish Swimming[END_REF]. Swimming speeds in fishes are commonly normalised to bodylengths s -1 (BL s -1 ) to facilitate comparison among individuals of different sizes. This does not in fact completely compensate for size effects because maximum swim speeds in BL s -1 decline significantly with length within and across fish species [START_REF] Bainbridge | The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat[END_REF][START_REF] Beamish | Swimming capacity[END_REF][START_REF] Videler | Fish Swimming[END_REF]. The cost of swimming increases exponentially with increasing speed, because the drag a fish must overcome when swimming increases with the square of the velocity [START_REF] Videler | Fish Swimming[END_REF]. There are various other factors that can contribute to the cost of swimming, for example the cost of gill ventilation, which may depend on the mode of ventilation and whether this changes with swimming speed [START_REF] Steffensen | The Transition between Branchial Pumping and Ram Ventilation in Fishes: Energetic Consequences and Dependence on Water Oxygen Tension[END_REF]. Furthermore, the increased ventilation and perfusion of the gills that is required to provide oxygen for aerobic swimming, will also result in increased ion and water movements across the respiratory epithelium, a phenomenon known as the osmo-respiratory compromise [START_REF] Randall | The relationship between gas and ion transfer across the gills of fishes[END_REF][START_REF] Gonzalez | the relationship between oxygen consumption and ion loss in a freshwater fish[END_REF][START_REF] Gallaugher | Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming[END_REF]. This may also contribute to an increased energy expenditure in exercising fish. The capacity of fishes to meet the costs of aerobic swimming is of course finite. The species-specific maximum capacity for aerobic swimming occurs at the maximum sustainable swimming speed (Ums), which is taken to mean a speed that can be sustained for hours or even days without fatigue [START_REF] Beamish | Swimming capacity[END_REF][START_REF] Blasco | Using aerobic exercise to evaluate sub-lethal tolerance of acute warming in fishes[END_REF][START_REF] Videler | Fish Swimming[END_REF]. The critical swimming speed (Ucrit) has often been considered a relatively close approximation of Ums in fishes [START_REF] Hammer | Lymphocyte recirculation, exercise, and immune responses[END_REF]. The Ucrit protocol involves imposing step-wise increases in speed in a swimtunnel, until the fish fatigues. The Ucrit exceeds Ums because fishes transition from steady (sustainable) aerobic swimming to unsteady (unsustainable) anaerobic swimming prior to fatigue. A number of studies suggest that the maximum speed that can be sustained aerobically corresponds to about 60-80% Ucrit [START_REF] Burgetz | Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss)[END_REF][START_REF] Lee | The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks[END_REF][START_REF] Wilson | Assessment of maximum sustainable swimming performance in rainbow trout[END_REF].

Within the range of aerobic speeds that a fish can swim at, the energy expenditure per distance travelled is often referred to as the cost of transportation (COT) [START_REF] Beamish | Swimming capacity[END_REF][START_REF] Davison | Swimming-Enhanced Growth[END_REF]. This is, however, slightly misleading because it includes metabolic costs that are unrelated to the cost of locomotion, such as SMR and even the SDA (Fig. 1a). At low and moderate swimming velocities, the cost of locomotion may be the smallest of these factors (Fig. 1a). In addition, a need for stability control at low speeds may also contribute to overall metabolic cost [START_REF] Fitzgibbon | Metabolic scope, swimming performance and the effects of hypoxia in the mulloway, Argyrosomus japonicus (Pisces: Sciaenidae)[END_REF]. The cost of transport is often specified as to whether or not it includes SMR, being either total cost of transport (TCOT) or net cost of transport (NCOT) respectively [START_REF] Ohlberger | Swimming efficiency and the influence of morphology on swimming costs in fishes[END_REF]; the latter is sometimes also called the cost of swimming (COS, McKenzie et al., 2003). The TCOT typically shows a 'U-shape' against swimming speed, the elevated TCOT at low speeds (Fig. 1b) is primarily due to the SMR occupying a large proportion of the total metabolic rate, with the cost of swimming being low (Fig. 1a). The swimming speed at which the TCOT is the lowest has been defined as the optimal swimming speed (Uopt, Fig 1b) [START_REF] Tucker | Energetic cost of locomotion in animals[END_REF][START_REF] Videler | Fish Swimming[END_REF]. It may be important for fishes when they are foraging, where energy acquired can be proportional to the distance travelled. The Uopt is influenced by environmental factors such as water temperature [START_REF] Claireaux | Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax)[END_REF] as well as by inherent characters of the fish, such as morphology, body size, nutritional and reproductive status [START_REF] Cai | Interrelationships between feeding, food deprivation and swimming performance in juvenile grass carp[END_REF][START_REF] Kaufmann | Respiratory Cost of Swimming in Larval and Juvenile Cyprinids[END_REF][START_REF] Pettersson | Energetics, cost reduction and functional consequences of fish morphology[END_REF]. In addition, schooling also reduces the cost of swimming [START_REF] Marras | Fish swimming in schools save energy regardless of their spatial position[END_REF]. There are reports that spontaneous preferred swimming speed of various species coincides with their Uopt (e.g. [START_REF] Tudorache | Optimal swimming speeds reflect preferred swimming speeds of brook charr (Salvelinus fontinalis Mitchill, 1874)[END_REF][START_REF] Weihs | Voluntary Swimming Speeds of Two Species of Large Carcharhinid Sharks[END_REF]. For farmed fishes, food is supplied in abundance and access to feed is not directly proportional to the distance covered. Thus, it could be argued that in an aquaculture context, any energy that is allocated to aerobic swimming does not promote food acquisition and therefore does not contribute to growth (Fig. 1a).

What swimming speed to choose?

Given the metabolic costs of aerobic swimming, and how these change with speed, the question that arises is what speed to impose in order to enhance or promote growth. The currents or swimming speeds reported to give the best growth of fishes, primarily based on studies of salmonids, are in the range of 0.5-1.7 bl•s -1 [START_REF] Davison | The Effects of Exercise Training on Teleost Fish[END_REF][START_REF] Davison | Training and its effects on teleost fish[END_REF][START_REF] Davison | Swimming-Enhanced Growth[END_REF][START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF]. Based on data from a number of salmonids and carangids, [START_REF] Davison | Swimming-Enhanced Growth[END_REF] proposed that the swimming speed at which optimal growth occurs should coincide with the Uopt (see Fig 8.4, Davison and Herbert, 2013). This raises the complicating factor of fish length, since smaller fishes swim at higher relative speeds and therefore have higher Uopt when normalised to BL s -1 [START_REF] Davison | Swimming-Enhanced Growth[END_REF]. The importance of size-related differences in Uopt has not received sufficient attention but is clearly of potential significance for applying exercise as a tool in aquaculture, including in terms of adjusting speeds as fishes grow. From the literature, it is evident that a large number of studies on effects of exercise on growth have been conducted on small fishes (Table 8.1 Davison and Herbert,and Table 1). This is a logical consequence of issues such as limited laboratory space, numbers and sizes of available tanks, and the cost of animals and feed, but means that much available information is about juveniles rather than animals approaching marketable size.

Fishes are active even when there is no current

The swimming speed of fishes is not always determined by the water current. Even if kept in still water, many species of fish will swim spontaneously and, under these conditions, their metabolic rate may be increased (Fig 2) to the extent that it is either equal to [START_REF] Christiansen | Oxygen-Consumption in Relation to Sustained Exercise and Social Stress in Arctic Charr (Salvelinus-Alpinus L)[END_REF] or higher than that of fish swimming steadily against a moderate current [START_REF] Skov | Effects of rearing density and water current on the respiratory physiology and haematology in rainbow trout, Oncorhynchus mykiss at high temperature[END_REF]. In fact, swimming spontaneously with a complex turning trajectory can be significantly more costly than swimming at the same speed but against a current and in a straight line [START_REF] Steinhausen | The effects of swimming pattern on the energy use of gilthead seabream ( Sparus aurata L.)[END_REF]. If not compensated for by increased energy intake, the increased metabolic rate would reduce growth (Fig. 2). In still water or at very low swimming speeds, increased activity levels of fishes can reflect increased levels of aggression, which disappear when a current is provided that stimulates shoaling or schooling [START_REF] Christiansen | The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise[END_REF][START_REF] Christiansen | Effects of Sustained Exercise on Growth and Body Composition of First-Feeding Fry of Arctic Charr[END_REF][START_REF] East | The effect of locomotor activity on the growth of brook charr, Salvelinus fontinalis Mitchill[END_REF]Jørgensen and Jobling, 1993). Aggression can result in reduced feed intake [START_REF] Christiansen | The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise[END_REF]Jørgensen and Jobling, 1993) and, as a result, reduced growth compared with fish swimming against a current at moderate velocities (Fig. 2). The spontaneous behaviour and aggressivity of fishes also depends on other factors, such as rearing density [START_REF] Christiansen | Oxygen-Consumption in Relation to Sustained Exercise and Social Stress in Arctic Charr (Salvelinus-Alpinus L)[END_REF]Jørgensen et al., 1993;[START_REF] Larsen | The effects of stocking density and low level sustained exercise on the energetic efficiency of rainbow trout (Oncorhynchus mykiss) reared at 19°C[END_REF][START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF] and access to feed [START_REF] Jørgensen | Food acquisition and growth of juvenile Atlantic salmon (Salmo salar) in relation to spatial distribution of food[END_REF], which can also affect their growth [START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF]. Overall, spontaneous swimming behaviour of fishes may be a significant factor in determining how a current influences growth rates [START_REF] Christiansen | The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise[END_REF][START_REF] Larsen | The effects of stocking density and low level sustained exercise on the energetic efficiency of rainbow trout (Oncorhynchus mykiss) reared at 19°C[END_REF][START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF][START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF].

Mechanisms for increased growth

It is possible that, in many studies, the positive effects of exercise on growth were simply derived from an increase in feed intake. In many early studies, feeding was unrestricted and feed intake was not reported, such that feed efficiency and FCR are not known. In this regard, it is interesting that beneficial effects of swimming exercise are often found when comparing fish kept in still water and those swimming at intermediate swimming velocities, 0.5 to 2 BL s -1 [START_REF] Davison | Swimming-Enhanced Growth[END_REF]. Swimming exercise can stimulate appetite (Fig. 2) to match the increased metabolic demands of locomotion, such that growth is not compromised or is even increased [START_REF] Christiansen | The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise[END_REF]Jørgensen and Jobling, 1993;[START_REF] Khan | Accommodating the cost of growth and swimming in fishâ€"the applicability of exercise-induced growth to juvenile hapuku (Polyprion oxygeneios)[END_REF][START_REF] Leon | Effect of Exercise on Feed Consumption, Growth, Food Conversion, and Stamina of Brook Trout[END_REF][START_REF] Li | The effect of aerobic exercise and starvation on growth performance and postprandial metabolic response in juvenile southern catfish (Silurus meridionalis)[END_REF][START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF][START_REF] Totland | Growth and composition of the swimming muscle of adult Atlantic salmon (Salmo salar L.) during long-term sustained swimming[END_REF]. In fact, fish species may be able to exercise constantly at velocities between 0.5 to 2 BL s -1 without any decline in growth rate, by compensating with increased feed intake. This, of course, implies progressively reduced feed efficiency and FCR as swimming speed increases [START_REF] Kiessling | Influence of Sustained Exercise at Two Ration Levels on Growth and Thyroid Function of All-Female Chinook Salmon ( Oncorhynchus tshawytscha ) in Seawater[END_REF][START_REF] Kiessling | Age, ration level, and exercise affect the fatty acid profile of chinook salmon (Oncorhynchus tshawytscha) muscle differently[END_REF][START_REF] Khan | Accommodating the cost of growth and swimming in fishâ€"the applicability of exercise-induced growth to juvenile hapuku (Polyprion oxygeneios)[END_REF][START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF]; Table 1).

It is conceivable, nonetheless, that FCR and growth 'efficiency' are improved in exercised fish compared with those held in still water [START_REF] Christiansen | The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise[END_REF][START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF][START_REF] Shrivastava | Exercise improves growth, alters physiological performance and gene expression in common carp (Cyprinus carpio)[END_REF]. Swimming exercise at moderate levels appears to stimulate various regulatory factors that affect feed intake or growth, such as the expression of growth hormone (GH) and insulin-like growth factor-1 (IGF-1) [START_REF] Barrett | Sustained Exercise Increases Plasma Growth Hormone Concentrations in Two Anadromous Salmonids[END_REF][START_REF] Blasco | Growth-promoting effects of sustained swimming in fingerlings of gilthead sea bream (Sparus aurata L.)[END_REF][START_REF] Shrivastava | Exercise improves growth, alters physiological performance and gene expression in common carp (Cyprinus carpio)[END_REF] as well as expression of various genes associated with growth processes (Palstra et al., 2010b). Moreover, protein turnover and deposition have been reported to increase in exercised fish compared with controls in still water [START_REF] Houlihan | Effects of Exercise Training on the Performance, Growth, and Protein Turnover of Rainbow Trout ( Salmo gairdneri )[END_REF]. It is also true, however, that improved FCR of fishes reared at moderate swimming speeds, compared with those in still water, could also result from reduced feed intake and/or higher metabolic rates of the latter group, for the behavioural reasons that we have outlined above. Indeed, few if any studies showing increased growth rates in moderately exercised fish have included detailed measurements of feed intake and metabolic rate.

Future directions and considerations

It is clear that further work is needed to understand how swimming exercise can be used to improve production in aquaculture. There is no consensus in the literature and it is not clear to what extent this reflects differences among species, in life stage and body size, in the swimming speed applied, the feeding regime, and so forth. Feed represents the major operational cost in fish farming and, in many instances, production is regulated by feed quotas or nutrient emission allowances. From this perspective, increased growth is only really interesting if it is linked to more efficient utilization of ingested feed. Thus, further research is needed to demonstrate that aerobic swimming improves FCR or protein retention in the species of interest, throughout rearing to market size. The best advice for which swimming speed to choose remains that this should be close to Uopt [START_REF] Davison | Swimming-Enhanced Growth[END_REF].

Research efforts on the effects of exercise should also consider diet formulation, in particular to increase non-protein energy to fuel the metabolic costs of swimming, such that dietary protein can be retained and allocated towards growth. [START_REF] Magnoni | Metabolic Fuel Utilization During Swimming: Optimizing Nutritional Requirements for Enhanced Performance[END_REF] emphasized the need for research into how dietary lipids and carbohydrates are used to fuel sustained swimming in fishes. There have been some studies investigating how swimming fish use fuels [START_REF] Kieffer | A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss)[END_REF][START_REF] Lauff | Effects of training on respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout (Oncorhynchus mykiss )[END_REF][START_REF] Liew | Fasting goldfish, Carassius auratus, and common carp, Cyprinus carpio, use different metabolic strategies when swimming[END_REF][START_REF] Richards | Substrate utilization during graded aerobic exercise in rainbow trout[END_REF]. The work of [START_REF] Alsop | The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss)[END_REF] demonstrated an increased reliance on nonprotein energy sources to fuel metabolism with increasing swimming speeds in rainbow trout (Oncorhynchus mykiss). [START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF] made a similar observation, noting that the nitrogen quotient in rainbow trout was reduced by 20% in trout swimming against a current at 1 BL s -1 , compared to trout held in still water (0 BL s -1 ). Although this was beneficial in reducing the relative reliance on protein as fuel, overall fuel use was higher in the trout held in a swimming current. Interestingly, carbohydrate may contribute 40% of the metabolic cost of swimming at intermediate speeds, despite carbohydrate only making up ~10% of the energy reserves of a fish [START_REF] Magnoni | Metabolic Fuel Utilization During Swimming: Optimizing Nutritional Requirements for Enhanced Performance[END_REF]. In studies by [START_REF] Ibarz | Sustained swimming improves muscle growth and cellularity in gilthead sea bream[END_REF] and Sánchez-Gurmaches et al. ( 2013), an increase in dietary carbohydrate content had beneficial effects on the growth of gilthead seabream (Sparus aurata) reared with a swimming current. This may be linked to increased uptake and use of carbohydrates as fuel in skeletal muscle, which promotes a protein-sparing effect, as reported for rainbow trout (Felip et al., 2012;[START_REF] Skov | No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime[END_REF]. Nutritional optimisation is, therefore, a topic that is certainly worthy of further investigation.

Exercise and mitigation: links with welfare

Welfare is an extremely important element of successful intensive aquaculture, being a broad concept that embraces both the physical and mental well-being of an animal. A pragmatic definition of 'good welfare' is that an animal is healthy and has what it 'wants' [START_REF] Dawkins | The Science of Animal Suffering[END_REF]. This definition encompasses the three alternative definitions of animal welfare [START_REF] Fraser | Understanding animal welfare[END_REF] based on function, feelings and nature, where animals should have positive natural experiences similar to those in the wild. In food production aquaculture, the function-based definition tends to dominate [START_REF] Huntingford | Current issues in fish welfare[END_REF], whereby basic biological functions like health, growth and reproduction are optimised under rearing conditions. There are a number of ways in which sustained aerobic exercise may promote welfare of farmed fishes, in terms of physical and mental well-being, and managing reproductive physiology.

Exercise and stress

There has been significant interest in whether exercise can improve welfare of intensively farmed fishes by alleviating stress, encouraged by the evidence that moderate aerobic exercise can provide relief against stress in mammals and humans [START_REF] Eliot | Aerobic exercise as a therapeutic modality in the relief of stress[END_REF][START_REF] Tsatsoulis | The protective role of exercise on stress system dysregulation and comorbidities[END_REF]. Stress, in its strictest sense, is an endocrine condition that indicates activation of the hypothalamic-pituitary axis that, in fishes, elicits a release of the steroid stress hormone cortisol. Stress can also, however, have a broader definition than the endocrine stress response; it can be considered to comprise any condition that causes deviations from homeostasis that can engender a decline in performance and welfare of animals [START_REF] Schreck | The Concept of Stress in Fish, First Edit[END_REF][START_REF] Schulte | What is environmental stress? Insights from fish living in a variable environment[END_REF]. Therefore, markers of 'stress' can include increased metabolic energy (and hence oxygen) demands or deviations in blood chemistry homeostasis, and reductions in 'fitness indicators' such as swimming performance itself, growth rates or tolerance of disease [START_REF] Schreck | The Concept of Stress in Fish, First Edit[END_REF][START_REF] Schulte | What is environmental stress? Insights from fish living in a variable environment[END_REF]. For fishes in aquaculture, it is widely recognised that factors such as non-optimal stocking densities or the formation of dominance hierarchies can cause chronic stress [START_REF] Barton | Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling[END_REF][START_REF] Schreck | The Concept of Stress in Fish, First Edit[END_REF]. It has also been suggested that not allowing active fishes, such as salmonids, the option to exercise against a current may, in itself, be intrinsically stressful [START_REF] Rodnick | The Stress and Stress Mitigation Effects of Exercise: Cardiovascular, Metabolic, and Skeletal Muscle Adjustments[END_REF].

Various studies have investigated whether providing a current to swim against can alleviate chronic stress in active fish species when reared in tanks, assessed as a reduction in circulating cortisol levels in blood. Table 2 shows the studies which have investigated how sustained aerobic exercise influences plasma cortisol in fishes. There is no clear picture that emerges, with exercise causing decreases, no change or even increases in circulating cortisol.

Clearly, the different responses may reflect the different species, current speeds and holding conditions, and the existing data allow no conclusions to be drawn about the potential impact of such factors. There is also an enduring debate about how to interpret plasma cortisol levels in fishes because of the complex feedback loops that can occur within endocrine responses [START_REF] Barton | Effects of chronic confinement on physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute handling[END_REF][START_REF] Schreck | The Concept of Stress in Fish, First Edit[END_REF].

It can be informative to evaluate how fish rearing conditions influence the ability to mount an acute stress response, as this reveals whether the HPI axis might have been downregulated by chronic stress [START_REF] Schreck | The Concept of Stress in Fish, First Edit[END_REF]. In the striped bass (Morone saxatilis), swimming lowered circulating levels of cortisol (Table 2) but did not influence the magnitude of the cortisol response to an acute handling stress [START_REF] Young | Effects of Exercise Conditioning on Stress Responses and Recovery in Cultured and Wild Young-of-the-Year Striped Bass, Morone saxatilis[END_REF]. In rainbow trout, sustained swimming either lowered [START_REF] Woodward | Exercise training and the stress response in rainbow trout, Salmo gairdneri Richardson[END_REF] or did not affect [START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF] circulating cortisol titres (Table 2) but, in both studies, there was no significant effect of swimming on the magnitude of the cortisol response to an acute stress. In matrinxà (Brycon amazonicus), sustained swimming lowered plasma cortisol titres [START_REF] Arbelaez-Rojas | Sustained swimming mitigates stress in juvenile Brycon amazonicus reared in high stocking densities[END_REF], although it had no effect on their cortisol response to transport stress [START_REF] Arbeláez-Rojas | Sustained Swimming Mitigates Stress in Juvenile Fish Brycon amazonicus[END_REF]. Thus, the evidence indicates that swimming has no chronic effects on sensitivity of the HPI axis to acute stress (Table 2.. There is strong evidence, however, that providing a current to swim against can accelerate recovery of plasma cortisol homeostasis after acute stresses such as exercise to exhaustion [START_REF] Milligan | Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout[END_REF], handling [START_REF] Young | Effects of Exercise Conditioning on Stress Responses and Recovery in Cultured and Wild Young-of-the-Year Striped Bass, Morone saxatilis[END_REF], confinement [START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF][START_REF] Veiseth | Accelerated recovery of Atlantic salmon (Salmo salar) from effects of crowding by swimming[END_REF] or live transport [START_REF] Arbelaez-Rojas | Sustained swimming mitigates stress in juvenile Brycon amazonicus reared in high stocking densities[END_REF].

Interestingly, the evidence that providing a current promotes more rapid recovery of plasma metabolites following exercise to exhaustion is more mixed. In some studies and species it did (e.g. [START_REF] Lackner | Responses of the intermediary metabolism to acute handling stress and recovery in untrained and trained Leuciscus Cephalus (Cyprinidae, Teleostei)[END_REF][START_REF] Milligan | Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout[END_REF][START_REF] Veiseth | Accelerated recovery of Atlantic salmon (Salmo salar) from effects of crowding by swimming[END_REF] whereas, in others, it did not [START_REF] Kieffer | The effects of low-speed swimming following exhaustive exercise on metabolic recovery and swimming performance in brook trout (Salvelinus fontinalis)[END_REF][START_REF] Meyer | An assessment of the use of low-level aerobic swimming in promoting recovery from handling stress in rainbow trout[END_REF][START_REF] Suski | Failure of low-velocity swimming to enhance recovery from exhaustive exercise in largemouth bass (Micropterus salmoides)[END_REF]. Exercise to exhaustion causes profound metabolic disturbances and should very rarely (or never) occur in aquaculture. The accelerated recovery of cortisol might be a training effect, where fishes that are exercised for extended periods develop greater scope for metabolism, that allows them to recover general homeostasis more rapidly [START_REF] Lackner | Responses of the intermediary metabolism to acute handling stress and recovery in untrained and trained Leuciscus Cephalus (Cyprinidae, Teleostei)[END_REF][START_REF] Mckenzie | Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout[END_REF].

To conclude, there is no clear support for the notion that providing a current during rearing can systemically alleviate endocrine 'stress' in fishes. A swimming current may, however, mitigate routine handling and transport stresses, by accelerating recovery of endocrine homeostasis.

Exercise and immunity

There is very limited knowledge regarding the impact of exercise regimes on the immune performance of farmed fishes, but this is an interesting area for research because of the severe impacts that disease can have on aquaculture operations. In mammals, it is now generally accepted that aerobic exercise improves immunocompetency, although intense exhaustive exercise may be immunosuppressive [START_REF] Campbell | Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan[END_REF]. In various mammalian species including humans, exercise influences disease resistance, the capacity to initiate a successful immune response to pathogens, and vaccination success [START_REF] Pascoe | The effects of exercise on vaccination responses: A review of chronic and acute exercise interventions in humans[END_REF]. One underlying mechanism may be that aerobic exercise stimulates leucocytosis and redistribution of leukocytes throughout the body. This redistribution has been linked to a heightened state of immune surveillance and immune regulation, which contributes to an increased resistance to infection [START_REF] Campbell | Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan[END_REF].

In fishes, [START_REF] Castro | Disease resistance is related to inherent swimming performance in Atlantic salmon[END_REF] reported that Atlantic salmon (Salmo salar) individuals with inherently good swimming performance displayed increased resistance to a viral infection, infectious pancreatic necrosis virus (IPNV). In the same experiment different training regimes did not, however, improve immune performance. That is, individual variation in swimming performance accounted for variation in disease resistance, rather than a training regime. A further study compared immune-related gene profiles in a wild versus a domesticated population of Atlantic salmon, that had been further classified into inferior or superior swimmers. This revealed complex differences in gene expression between the populations but there was no link to inherent swimming performance nor any specific pattern of response to the training regime [START_REF] Robinson | Training the salmon's genes: influence of aerobic exercise, swimming performance and selection on gene expression in Atlantic salmon[END_REF].

In mammals, it is highly likely that cell mobilisation and redistribution throughout the body during exercise significantly contributes to any subsequent changes in tissue immunerelated gene expression [START_REF] Campbell | Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan[END_REF]. It has proven difficult to understand the tissue distribution of the various cells of the immune response, and their capacity for mobilisation and redistribution [START_REF] Campbell | Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan[END_REF][START_REF] Hammer | Lymphocyte recirculation, exercise, and immune responses[END_REF]. Thus, if gene expression data from mammals must be interpreted with caution, the situation is even less favourable for studies of effects of exercise on fishes. There is a very limited toolbox for accurate cellular phenotyping to analyse populations of leukocytes and their tissue distributions. This, coupled with our limited understanding of immune system dynamics during exercise, represents a bottleneck in our current capacity to interpret data in fishes.

It is worthwhile to mention that exercise, both acute and chronic, has a beneficial adjuvant-type effect on the immune response to vaccination in mammals [START_REF] Pascoe | The effects of exercise on vaccination responses: A review of chronic and acute exercise interventions in humans[END_REF].

Interestingly, this has been attributed to cytokine release including interleukin-6 (IL-6), and to tissue damage, particularly muscle damage [START_REF] Bruunsgaard | Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage[END_REF]. A recent study in zebrafish (Danio rerio) identified increased expression of IL-6 in certain muscle fibres in response to exercise [START_REF] Rovira | Exercise-Induced Hypertrophic and Oxidative Signaling Pathways and Myokine Expression in Fast Muscle of Adult Zebrafish[END_REF]. These observations suggest that exercise regimes may have potential to increase the effectiveness of vaccination in commercially farmed fish species, by a similar beneficial adjuvant-like effect.

Exercise, cognition and neural plasticity

Given the desire to ensure optimal welfare in intensively-farmed fishes, there has been interest in whether stimulating aerobic exercise with a current can promote neurogenesis, neuroplasticity and cognition [START_REF] Huntingford | Exercise, Stress and Welfare[END_REF]. Such effects of exercise are well-established in mammals [START_REF] Cotman | Exercise: a behavioral intervention to enhance brain health and plasticity[END_REF][START_REF] Van Praag | Neurogenesis and Exercise: Past and Future Directions[END_REF]. In adult rodents, for example, voluntary exercise promotes neurogenesis and expression of neurotrophins, particularly in the hippocampus [START_REF] Cotman | Exercise: a behavioral intervention to enhance brain health and plasticity[END_REF][START_REF] Soya | BDNF induction with mild exercise in the rat hippocampus[END_REF]. The hippocampus plays an important role in relational memory and spatial orientation [START_REF] Broglio | Hippocampal Pallium and Map-Like Memories through Vertebrate Evolution[END_REF] and exercised mammals show increased cognitive performance in maze tests compared to sedentary conspecifics [START_REF] Ma | Physical exercise induces hippocampal neurogenesis and prevents cognitive decline[END_REF][START_REF] Van Praag | Neurogenesis and Exercise: Past and Future Directions[END_REF][START_REF] Vaynman | Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition[END_REF]. While neurogenesis in the adult mammalian brain occurs at relatively low rates and only in discrete brain areas, fishes exhibit neurogenesis in a multitude of brain areas throughout their livespan [START_REF] Zupanc | Neurogenesis and neuronal regeneration in the adult fish brain[END_REF][START_REF] Zupanc | Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish[END_REF]. This fact was a particular stimulus for investigating whether exercise-induced enhancement of neurogenesis and cognition also occurs in fishes [START_REF] Huntingford | Exercise, Stress and Welfare[END_REF].

Recent studies have confirmed that exercise can promote neurogenesis and neuroplasticity in juvenile Atlantic salmon. Eight weeks of voluntary sustained swimming caused upregulation of genes involved with neuronal signalling, cell proliferation and neurite outgrowth in the telencephalon transcriptome [START_REF] Mes | Swimming exercise enhances brain plasticity in fish[END_REF]. Furthermore, increased expression of a neurogenesis marker, proliferating cell nuclear antigen (pcna), plus two neuroplasticity markers, synaptotagmin (syt) and brain-derived neurotrophic factor (bdnf), was found in specific areas of the telencephalon in the exercised group [START_REF] Mes | Swimming exercise enhances brain plasticity in fish[END_REF]. In the brain of zebrafish larvae, a six-day intermittent training regime increased expression of two genes involved in neurogenesis, cell differentiation and cell growth [START_REF] Fiaz | Exploring the effect of exercise on the transcriptome of zebrafish larvae ( Danio rerio )[END_REF].

Interestingly, exercise-enhanced expression of neuroplasticity markers has been observed in multiple areas of the telencephalon of exercised fish and does not seem to be confined to the dorsolateral pallium, which in fishes is the functional equivalent of the mammalian hippocampus.

To date, little is known about the effects of swimming exercise on cognition in fishes.

A 20-day exhaustive swimming exercise regime improved associative learning performance in a conditioning test in zebrafish [START_REF] Luchiari | Physical exercise improves learning in zebrafish, Danio rerio[END_REF]. However, neither three nor eight weeks of voluntary sustained swimming improved the cognitive performance of Atlantic salmon parr in a maze test, despite increased expression of neuroplasticity markers in their telencephalon [START_REF] Mes | Brain training: Can swimming exercise promote brain plasticity and cognitive performance in Atlantic salmon?[END_REF].

Overall, the existing findings suggest that, although exercise can promote neural plasticity in teleosts, there is little evidence for an associated increase in cognition. This is an interesting area for future research, in particular with a comprehensive approach that evaluates both neuroplasticity markers and cognitive performance in the same experiment. A particular focus should be upon enhancing cognition in animals that will be used in stocking programs, because hatchery-reared fish are often behaviourally naïve and consequently have low survival rates when released into the wild [START_REF] Jonsson | Restoration and Enhancement of Salmonid Populations and Habitats with Special Reference to Atlantic Salmon[END_REF][START_REF] Thorstad | Low survival of hatchery-released A Atlantic salmon smolts during initial river and fjord migration[END_REF].

Exercise and sexual maturation

Precocious maturation is a significant problem for many important aquaculture species, notably European sea bass (Dicentrarchus labrax) [START_REF] Felip | Reduction of sexual maturation in male Dicentrarchus labrax by continuous light both before and during gametogenesis[END_REF], gilthead seabream [START_REF] Gines | Growth in adult gilthead sea bream (Sparus aurata L) as a result of interference in sexual maturation by different photoperiod regimes[END_REF], Atlantic cod (Gadus morhua) [START_REF] Taranger | Continuous light delays sexual maturation and increases growth of Atlantic cod (Gadus morhua L.) in sea cages[END_REF] and Atlantic salmon [START_REF] Good | A Review of Factors Influencing Maturation of Atlantic Salmon, Salmo salar , with Focus on Water Recirculation Aquaculture System Environments[END_REF]. As fishes grow, the transition from the juvenile phase, characterised by extensive somatic growth, to a mature adult phase characterized by gonadal recrudescence and spawning, involves a major change in patterns of energy allocation. Energy investments in early maturation may negatively impact growth performance, feed conversion efficiency, fillet quality and the development of the immune system and, consequently, cause important economic losses.

Although the exact mechanisms that trigger this transition in energy allocation are still not known, it has been suggested that swimming exercise may play an important role in suppressing sexual maturation. This is because fish species that exhibit lengthy reproductive migrations show delayed or even arrested gonadal development during the migration itself.

Such long-distance migrants show swimming-induced suppression of ovarian development at the start of vitellogenesis (or puberty), which may be a strategy to avoid increased drag resistance due to oocyte growth and to prevent precocious muscle atrophy. When female European eels (Anguilla anguilla) were subjected to long-term sustained exercise, declines in mRNA expression of estrogen receptor 1, vitellogenin1 and vitellogenin2 in the liver indicated suppression of hepatic vitellogenesis (Palstra et al., 2010a;Palstra and van den Thillart, 2010). Furthermore, when appropriate photothermal conditions were mimicked during a simulated migration, European eel ovaries advanced their previtellogenic development but did not initiate vitellogenesis [START_REF] Mes | Simulated migration under mimicked photothermal conditions enhances sexual maturation of farmed European eel (Anguilla anguilla)[END_REF]. Female rainbow trout subjected to long-term exercise showed suppressed oocyte development, possibly through inhibition of vitellogenin uptake (Palstra et al., 2010a). A concomitant downregulation of transcriptomic responses in the ovary indicated that the energetic strategy was focussed on migration rather than sexual maturation. Thus, sustained exercise can delay gonadal development in various migratory fish species.

This has stimulated research into whether a sustained exercise regime can prevent precocious maturation in farmed fishes. [START_REF] Graziano | Swimming exercise to control precocious maturation in male seabass (Dicentrarchus labrax)[END_REF] showed that exercise at Uopt resulted in delayed testicular development in male European sea bass. The gonado-somatic index was lower, testicular development was delayed and the expression of genes involved in testicular development was down-regulated in exercised as compared to non-exercised fish. [START_REF] Waldrop | The effects of swimming exercise and dissolved oxygen on growth performance, fin condition and precocious maturation of early-rearing Atlantic salmon Salmo salar[END_REF] found that male Atlantic salmon exercised at swimming speeds of 1.5 to 2.0 BL s -1 showed significantly less precocious maturation than those swimming at a speed lower than 0.5 BL s -1 (6.5% and 11.5%, respectively).

Therefore, exercise may be a promising tool to reduce the incidence of sexual precociousness in aquaculture and this is a particularly interesting area for future research.

Notably, to investigate fundamental questions such as the mechanisms by which sustained aerobic exercise suppresses sexual maturation in fishes. For example, in coho salmon (Oncorhynchus kisutch) and rainbow trout (Barrett andMcKeown, 1989, 1988), exercise can enhance plasma levels of GH and, in gilthead seabream, it raises plasma IGF-I levels [START_REF] Sánchez-Gurmaches | Insulin, IGF-I, and muscle MAPK pathway responses after sustained exercise and their contribution to growth and lipid metabolism regulation in gilthead sea bream[END_REF]. This stimulation of growth factors may prevent the transition from a juvenile life stage, governed by the GH/IGF axis, to a reproductive stage governed by the brain-pituitary-gonadal axis, a switch that is often preceded by a drop in GH.

Swimming behaviours as Operational Welfare Indicators

Swimming and the activities that it underpins are obviously natural behaviours that can promote 'good welfare' so, ideally, captive fishes should be allowed to express them without restrictions. Behavioural swimming patterns and responses are good OWI that provide information about the welfare of groups of fish under culture conditions, rather than about single individuals. Swimming activity provides good OWI that, for a given species, may comprise different patterns and space requirements at different life stages. The movement and orientation of larvae can provide guidance for welfare, especially during weaning when it can reflect yolk sac depletion and first feeding. A good OWI would be the proportion of fish orientating and migrating to the surface to feed actively. Fishes start swimming actively after weaning and, therefore, swimming patterns in the tank, alongside horizontal and vertical distributions, are also a useful OWI. Interpreting movement paterns requires knowledge of the species, Shoaling or schooling in the tank may indicate good welfare, rather than chaotic movements and clumped distribution indicative of anxiety like behaviour and stress responses. Tight shoals can, however, be induced by fear of predation, which may indicate an underlying stress response. In tank systems for salmonids, the water flow rate should ideally allow the fish to 'hold station', a natural behaviour for these species. Increasing the flow rate so that fish shoal and swim actively against a current can also mitigate against agonistic behaviours, as discussed earlier. This provides an OWI because agonistic behaviours can reduce welfare by causing stress and fin damage [START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF].

Exercise and selection: creating more robust strains?

Little is known about the genetic basis of swimming performance in fishes, and whether there might be genetic correlations with traits of interest for production. In terrestrial livestock, selection for production traits has been shown to lead to various disorders including cardiac failures in intensely selected lines [START_REF] Nestor | Direct and correlated responses to longterm selection for increased body weight and egg production in turkeys[END_REF][START_REF] Rauw | Undesirable side effects of selection for high production efficiency in farm animals: a review[END_REF]. Thus, it has been suggested that the occurrence of cardiac malformations and failures in some lines of farmed salmonids [START_REF] Mercier | Cardiac disorders in farmed adult brown trout, Salmo trutta L[END_REF][START_REF] Poppe | Suspected myocardial necrosis in farmed Atlantic salmon, Salmo salar L.: a field case[END_REF] could similarly be linked to prioritising growth rate in selective breeding. In rainbow trout selected for rapid growth, individual swimming performance was a predictor of cardiac morphology and pumping ability [START_REF] Claireaux | Linking swimming performance, cardiac pumping ability and cardiac anatomy in rainbow trout[END_REF]. It has been suggested, therefore, that swimming performance phenotype could potentially be selected upon, to improve the functional integrity of farmed fish that have previously been selected for rapid growth. There are, however, very few studies that have investigated the genetic basis of swimming ability.

Heritability measures the fraction of phenotypic variance that can be attributed to genetic variation and ranges from 0 (none can be attributed) to 1 (all is attributed). In brown trout (Salmo trutta) and Atlantic salmon, heritability of Ucrit was moderate with large error terms, namely 0.34 ± 0.22 [START_REF] Blanc | Variabilité génétique de la performance de nage chez l'alevin de Truite fario (Salmo trutta)[END_REF] and 0.24 ± 0.16 [START_REF] Hurley | Genetic control of swimming stamina in Atlantic salmon ( Salmo salar )[END_REF], respectively. Similar heritability estimates of 0.24 ± 0.19 were reported for the guppy Poecilia reticulata Peters 1859 [START_REF] Nicoletto | Offspring quality and female choice in the guppy,Poecilia reticulata[END_REF]. In the threespine stickleback Gasterosteus aculeatus L. 1756, heritability of burst swimming speed was relatively high at two months of age (0.37-0.41) but had fallen to almost zero at 3.6 months in the same individuals, raising questions about the validity of the results [START_REF] Garenc | Burst swimming and its enzymatic correlates in the threespine stickleback ( Gasterosteus aculeatus ): full-sib heritabilities[END_REF]. In the European sea bass, heritability of relative maximum burst swimming speed (in BL s -1 ) was quite high, at 0.55 ± 0.08 [START_REF] Vandeputte | Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax)[END_REF], with a very high (0.96) genetic correlation between two independent evaluations of the trait, on the same fish at 5-day intervals.

Genetic correlations between swimming performance and other traits have been studied very little. There were weak positive correlations (0.23) between absolute maximum sustained swimming speed and body mass in Atlantic salmon [START_REF] Hurley | Genetic control of swimming stamina in Atlantic salmon ( Salmo salar )[END_REF] and in European sea bass (0.12; [START_REF] Vandeputte | Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax)[END_REF]. In European sea bass, maximum swimming speed in BL s -1 was negatively correlated with body mass, and this was true of all genetic (-0.64), phenotypic (-0.56) and environmental (-0.45) correlations [START_REF] Vandeputte | Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax)[END_REF]. This suggests that the negative relationship between body size and relative swimming speed is purely phenotypic, as has already been established in fishes [START_REF] Bainbridge | The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat[END_REF][START_REF] Beamish | Swimming capacity[END_REF][START_REF] Bellwood | Relative swimming speeds in reef fish larvae[END_REF]. In European sea bass, there was a weak negative genetic correlation (-0.10 ± 0.19) but no phenotypic correlation (0.01) between relative swimming speed and cortisol response to confinement stress, indicating that these two traits are independent in this species [START_REF] Vandeputte | Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax)[END_REF]. The same study also found no difference in relative or absolute swimming speed between the offspring of wild, domesticated (1 generation) or growth selected (1 generation) parents, confirming moderate links between swimming capacity and the genetic bases of growth. Thus, keeping in mind what has been observed in terrestrial livestock, it is possible that selection for growth degrades swimming ability and underlying cardiac performance, over successive generations, but further investigation is needed to demonstrate genetic links between these traits. Nonetheless, due to the moderate to high heritability of swimming capacity, selecting fish for improved exercise performance could be a simple way to counteract any negative effects of selection for fast growth. It may also be a means of ensuring that robust animals with good exercise performance are used in restocking programs, to promote their survival [START_REF] Jobling | The effects of prolonged exercise training on growth performance and production parameters in fish[END_REF][START_REF] Thorstad | Low survival of hatchery-released A Atlantic salmon smolts during initial river and fjord migration[END_REF].

Conclusions

Despite a great deal of interest from the aquaculture research community, it remains to be explicitly demonstrated that swimming exercise can actually 'promote' growth and improve feed efficiency, except through modifications to behaviour. There is also no consensus about whether swimming exercise can mitigate chronic stress in all species. Whether exercise can promote immunity and cognition is an interesting question that is worth exploring further, because there are clear potential applications in terms of welfare of farmed fishes. The evidence that exercise can inhibit precocious sexual maturation is also very promising, so this is another area where research should be encouraged. The use of swimming behaviour as OWI is of clear potential value to the fish farmer, especially for early life stages, so further studies on a broader range of species would be valuable. Finally, using exercise to select robust phenotypes, or to counteract debilitating effects of a historical selection for rapid growth, also requires further investigation. Overall, therefore, further research is required, in concert with fish farmers, to develop methods to exercise fishes in culture, or to use exercise as a selection tool.

Table 1. Studies that have investigate the effects of forced aerobic swimming on growth performance in non-salmonid finfish species. The table carries information about initial body mass (BM), initial forklength (LI, when reported), swim speed (U), fish per tank (Tank), Temperature (T), feed intake (FI, when reported); feeding protocol (FP), feed conversion (FCR, when reported), specific growth rate (SGR), and the associated literature reference. R , is assumed to be constant at all swimming velocities. The cost of swimming increases exponentially with swimming velocity and the curve is derived from Webb (1971).

The specific dynamic action (SDA, the metabolic cost of digesting and assimilating a meal) is assumed to be maintained at all swimming velocities [START_REF] Alsop | The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss)[END_REF]Thorarensen & Farrell, 2006) for growth in fish. At low velocities feed intake ① may or may not be reduced, and/or metabolic rate increased ②, due to increased levels of spontaneous activity or aggression. As a result, the scope for growth is reduced. If neither feed intake is reduced nor metabolic rate increased, scope for growth is maintained over different swimming velocities and there is no effect of swimming exercise on growth. At swimming velocities above 45-50% of the maximum sustained swimming speed (Ums) growth is reduced because feed intake cannot meet the increased metabolic demands of swimming, and/or because feed intake is reduced ③.

Figure 1 .

 1 Figure 1. a) Schematic picture showing different components of metabolic rate in fishes as swimming speed increases up to Ums (maximum sustained swimming speed). The standard metabolic rate (SMR, the basal metabolic rate of ectothermic species at their acclimation temperature), is assumed to be constant at all swimming velocities. The cost of swimming

  . b) The Cost of Transportation (COT, the energy consumed while swimming one metre) is calculated based on the values in Fig 1a.

Figure 2 .

 2 Figure 2. A conceptual model of the interplay among metabolic rate, feed intake and scope

Table 2 .

 2 -1 ; C, circular; F, flume; AL, ad-libitum; RE, restricted; FCR calculated as feed mass/body mass gain. Studies that have investigated effects of chronic (days to months) sustained swimming exercise on circulating levels of cortisol in 991 fishes. 992

		Order,										Reference
	Species	Family	BMI	BMF	LI	U	Tank	T	FI	FP	FCR SGR
			(g)	(g)	(mm)	(BL s -1 )		(°C) (g day -1 )		(g day -1 )
		Perciformes
	Sparus											(Ibarz et al.,
	aurata	Sparidae	88±1	98±2		0	200C	20	2.6	AL	0.61	2011)
			90±1	107±2		1.5	400C	20	2.8	AL	0.76
												(Blasco et al.,
			5.0±0.1	14.5±0.5		0	200C	23		AL	1.17 3.41	2015)
			5.1±0.2	20.3±0.4		5	400C	23		AL	0.93 3.72
												(Felip et al.,
			50-60	70±2		0	200C	22	3.56±0.20	AL	1.13±0.05	2012)
			50-60	74±2		1.5	400C	22	3.84±0.03	AL	1.32±0.06
	Pagrus											(Forster and
	major	Sparidae	2.5±0.5	13.8		0	35C	27.5 3.16	AL ×2	0.81 4.4	Ogata, 1996)
			2.5±0.5	13.8		1.5	35C	27.5 3.16	AL ×2	0.83 4.5
			2.5±0.5	12.7		3.0	35C	27.5 2.92	AL ×2	0.79 4.2
			2.5±0.5	14.7		0	35C	27.5 3.25	AL ×2	0.81 4.6
			2.5±0.5	15.2		1.5	35C	27.5 3.03	AL ×2	0.75 4.6
			2.5±0.5	12.2		3.0	35C	27.5 3.40	AL ×2	0.94 4.1