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

Simon Mackenzie, Arjan Palstra, Josep Planas, David J Mckenzie, Marie-laure Bégout, Helgi Thorarensen, Marc Vandeputte, Daan Mes, Sonia Rey, Gudrun de Boeck, et al.

► To cite this version:

Simon Mackenzie, Arjan Palstra, Josep Planas, David J Mckenzie, Marie-laure Bégout, et al. Aerobic swimming in intensive finfish aquaculture: applications for production, mitigation and selection. Reviews in Aquaculture, 2020, 13 (1), pp.138-155. 10.1111/raq.12467. hal-03097375

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

3

4 D.J. McKenzie¹*, A. Palstra², J. Planas³, S. MacKenzie⁴, M.-L. Bégout⁵, H. Thorarensen⁶, M.

5 Vandeputte⁷,⁵, D. Mes⁸, S. Rey⁴, G. De Boeck⁹, P. Domenici¹⁰ and P.V. Skov¹¹.

6

7 ¹ MARBEC, Université Montpellier, CNRS, IRD, Ifremer, Montpellier, France

8 ² Wageningen University & Research Animal Breeding and Genomics, Wageningen Livestock

9 Research, Wageningen, The Netherlands

10 ³Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

11 ⁴ Institute of Aquaculture, University of Stirling, FK9 4LA Stirling, UK

12 ⁵ Ifremer, Chemin de Maguelone, Palavas-les-Flots, France

13 ⁶ Hólar University College, Sauðárkrókur, Iceland

14 ⁷ Université Paris-Saclay, INRAE, AgroParisTech, GABI, Jouy-en-Josas, France

15 ⁸ Department of Production Animal Clinical Sciences, Norwegian University of Life

16 Sciences, Oslo, Norway

17 ⁹ Systemic Physiological and Ecotoxicological Research, Department of Biology, University
18 of Antwerp, Antwerp, Belgium

19 ¹⁰ IAS-CNR, Istituto per lo studio degli impatti Antropici e Sostenibilità in ambiente marino,
20 Sezione di Oristano, Località Sa Mardini, Torregrande (Oristano), Italy

21 ¹¹ DTU Aqua, Section for Aquaculture, The North Sea Research Centre, Technical University
22 of Denmark, Hirtshals, Denmark

23

24 * david.mckenzie@cnrs.fr

25

26
27 Abstract

28 We review knowledge on applications of sustained aerobic swimming as a tool to promote
29 productivity and welfare of farmed fish species. There has been extensive interest in whether
30 providing active species with a current to swim against can promote growth. The results are
31 not conclusive but the studies have varied in species, life stage, swimming speed applied,
32 feeding regime, stocking density, and other factors. Therefore, much remains to be understood
33 about mechanisms underlying findings of 'swimming-enhanced growth', in particular to
34 demonstrate that swimming can improve feed conversion ratio and dietary protein retention
35 under true aquaculture conditions. There has also been research into whether swimming can
36 alleviate chronic stress, once again on a range of species and life stages. The evidence is
37 mixed but swimming does improve recovery from acute stresses such as handling or
38 confinement. Research into issues such as whether swimming can improve immune function
39 and promote cognitive function is still at an early stage and should be encouraged. There is
40 promising evidence that swimming can inhibit precocious sexual maturation in some species,
41 so studies should be broadened to other species where precocious maturation is a problem.

42 Swimming performance is a heritable trait and may prove a useful selection tool, especially if
43 it is related to overall robustness. More research is required to better understand the
44 advantages that swimming may provide to the fish farmer, in terms of production, mitigation
45 and selection.
46 **Introduction**

47 The aquaculture research community is interested in the potential applications of swimming
48 exercise as a tool to promote the productivity and welfare of some intensively farmed fish
49 species. This interest crystallized as an EU COST Action (FA1304 Fitfish) that provided a
50 forum to discuss the potential uses of exercise in finfish aquaculture. A critical reappraisal of
51 the literature is now timely (Palstra and Planas, 2013), so this review provides a concise
52 analysis of current knowledge focussing on three major applications for swimming, namely
53 production, mitigation and selection.

54 With regard to production, sustained aerobic exercise has been reported to stimulate
55 growth and/or improve feed conversion for a variety of farmed species, under experimental
56 conditions (Davison and Herbert, 2013). This is of obvious potential interest, we review the
57 latest evidence and the potential underlying mechanisms, which range from animal behaviour
58 (Jørgensen and Jobling, 1993; Skov et al., 2011) to muscle cell biology (Ibarz et al., 2011). In
59 terms of mitigating the deleterious impacts of intensive aquaculture on the welfare of fishes,
60 exercise has been reported to alleviate chronic stress (Young and Cech, 1993) and to promote
61 recovery from acute stresses (McKenzie et al., 2012; Milligan et al., 2000). It may also
62 improve disease resistance (Castro et al., 2011), promote neuroplasticity and cognition (Mes
63 et al., 2020), and inhibit precocious sexual maturation (Graziano et al., 2018; Palstra et al.,
64 2010a). We review the evidence for these positive effects and their underlying mechanisms.
65 We briefly consider how observation of swimming behaviour may provide ‘operational
66 welfare indicators’ (OWI), especially in early life stages.

67 In terms of using exercise as a tool for selection, this could have various applications.
68 Exercise tests may be useful in identifying robust animals within a population that are best
69 suited for grow out, for example for transfer to sea pens, and may be able to distinguish fish
70 for their stress coping styles. Exercise tests could also be used for trans-generational selection
71 of robust families, so we review the evidence that exercise performance is a heritable trait in
72 fishes (Vandeputte et al., 2016).

73 **Exercise and production: effects on growth**

74 Studies on the effects of exercise training on growth in fishes arose initially to resolve the
75 question of whether fish muscle displayed the same degree of plasticity as their mammalian
76 counterparts, when subjected to an exercise regime (Davison, 1989). Several parallel fields of
77 fundamental research examined how swimming exercise (and 'training') might affect variables
such as muscle fibre sizes and densities (Davison and Goldspink, 1977; Rasmussen et al., 2011), overall exercise performance capacity (Gallagher et al., 2001), and the use of metabolic fuels (Alsop and Wood, 1997; Richards et al., 2002). 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 (Davison, 1997, 1989; Davison and Herbert, 2013; 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. Ibarz et al., 2011; Palstra et al., 2015; Shrivastava et al., 2018), other studies have found that swimming exercise has no, or even negative, effects on growth (e.g. Kiessling et al., 1994; McKenzie et al., 2012; Skov et al., 2015).

## Growth and energy balance

At its most basic definition, growth is an increase in body mass due to consumption of food (Jobling, 2002). 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 (Brett, 1976; Brett and Groves, 1979; Jobling, 2002; Jobling et al., 1993).

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; Webb, 1998; McKenzie, 2011). 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 (Bainbridge, 1958; Beamish, 1978; Videler, 1993). 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 (Videler, 1993). 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 (Steffensen, 1985). 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 (Randall et al., 1972; Gonzalez & McDonald, 1992; Gallaugher et al., 2001). 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 (Beamish, 1978; Blasco et al., 2020; Videler, 1993). The critical swimming speed (Ucrit) has often been considered a relatively close approximation of Ums in fishes (Hammer, 1995). The Ucrit protocol involves imposing step-wise increases in speed in a swim-tunnel, 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 (Burgetz et al., 1998; Lee et al., 2003; Wilson and Egginton, 1994).

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) (Beamish, 1978; Davison and Herbert, 2013). 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 (Fitzgibbon et al., 2007). The cost of transport is often specified as to whether or not it includes SMR, being either total cost of transport ($T_{COT}$) or net cost of transport ($N_{COT}$) respectively (Ohlberger et al., 2006); the latter is sometimes also called the cost of swimming (COS, McKenzie et al., 2003). The $T_{COT}$ typically shows a 'U-shape' against swimming speed, the elevated $T_{COT}$ 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 $T_{COT}$ is the lowest has been defined as the optimal swimming speed ($U_{opt}$, Fig 1b) (Tucker, 1970; Videler, 1993). It may be important for fishes when they are foraging, where energy acquired can be proportional to the distance travelled. The $U_{opt}$ is influenced by environmental factors such as water temperature (Claireaux et al., 2006) as well as by inherent characters of the fish, such as morphology, body size, nutritional and reproductive status (Cai et al., 2014; Kaufmann, 1990; Pettersson and Hedenström, 2000). In addition, schooling also reduces the cost of swimming (Marras et al., 2015). There are reports that spontaneous preferred swimming speed of various species coincides with their $U_{opt}$ (e.g. Tudorache et al., 2011; Weihs et al., 1981). 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 (Davison, 1997, 1989; Davison and Herbert, 2013; Jobling et al., 1993). Based on data from a number of salmonids and carangids, Davison and Herbert (2013) proposed that the swimming speed at which optimal growth occurs should coincide with the $U_{opt}$ (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 $U_{opt}$ when normalised to BL s⁻¹ (Davison and Herbert, 2013). The importance of size-related differences in $U_{opt}$ 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.

## 179 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 (Christiansen et al., 1991) or higher than that of fish swimming steadily against a moderate current (Skov et al., 2011). 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 (Steinhausen et al., 2010). 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 (Christiansen and Jobling, 1990; Christiansen et al., 1989; East and Magnan, 1987; Jørgensen and Jobling, 1993). Aggression can result in reduced feed intake (Christiansen and Jobling, 1990; 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 (Christiansen et al., 1991; Jørgensen et al., 1993; Larsen et al., 2012; McKenzie et al., 2012) and access to feed (Jørgensen et al., 1996), which can also affect their growth (Jobling et al., 1993). Overall, spontaneous swimming behaviour of fishes may be a significant factor in determining how a current influences growth rates (Christiansen and Jobling, 1990; Larsen et al., 2012; McKenzie et al., 2012; Skov et al., 2015).

## 200 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
205 fish kept in still water and those swimming at intermediate swimming velocities, 0.5 to 2 BL
206 s⁻¹ (Davison and Herbert, 2013). Swimming exercise can stimulate appetite (Fig. 2) to match
207 the increased metabolic demands of locomotion, such that growth is not compromised or is
208 even increased (Christiansen and Jobling, 1990; Jørgensen and Jobling, 1993; Khan et al.,
209 2014; Leon, 1986; Li et al., 2016; Skov et al., 2015; Totland et al., 1987). In fact, fish species
210 may be able to exercise constantly at velocities between 0.5 to 2 BL s⁻¹ without any decline in
211 growth rate, by compensating with increased feed intake. This, of course, implies
212 progressively reduced feed efficiency and FCR as swimming speed increases (Kiessling et al.,
213 1994, 2005; Khan et al., 2014; Skov et al., 2015; Table 1).

214 It is conceivable, nonetheless, that FCR and growth 'efficiency' are improved in
215 exercised fish compared with those held in still water (Christiansen and Jobling, 1990; Jobling
216 et al., 1993; Shrivastava et al., 2018). Swimming exercise at moderate levels appears to
217 stimulate various regulatory factors that affect feed intake or growth, such as the expression of
218 growth hormone (GH) and insulin-like growth factor-1 (IGF-1) (Barrett and McKeown, 1988;
219 Blasco et al., 2015; Shrivastava et al., 2018) as well as expression of various genes associated
220 with growth processes (Palstra et al., 2010b). Moreover, protein turnover and deposition have
221 been reported to increase in exercised fish compared with controls in still water (Houlihan and
222 Laurent, 1987). It is also true, however, that improved FCR of fishes reared at moderate
223 swimming speeds, compared with those in still water, could also result from reduced feed
224 intake and/or higher metabolic rates of the latter group, for the behavioural reasons that we
225 have outlined above. Indeed, few if any studies showing increased growth rates in moderately
226 exercised fish have included detailed measurements of feed intake and metabolic rate.

227 **Future directions and considerations**

228 It is clear that further work is needed to understand how swimming exercise can be used to
229 improve production in aquaculture. There is no consensus in the literature and it is not clear to
230 what extent this reflects differences among species, in life stage and body size, in the
231 swimming speed applied, the feeding regime, and so forth. Feed represents the major
232 operational cost in fish farming and, in many instances, production is regulated by feed quotas
233 or nutrient emission allowances. From this perspective, increased growth is only really
234 interesting if it is linked to more efficient utilization of ingested feed. Thus, further research is
235 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 $U_{opt}$ (Davison and Herbert, 2013).

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. Magnoni et al. (2013) 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 (Kieffer et al., 1998; Lauff and Wood, 1997; Liew et al., 2012; Richards et al., 2002). The work of Alsop and Wood (1997) demonstrated an increased reliance on non-protein energy sources to fuel metabolism with increasing swimming speeds in rainbow trout (*Oncorhynchus mykiss*). Skov et al. (2015) 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 (Magnoni et al., 2013). In studies by Ibarz et al. (2011) 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; Skov et al., 2015). Nutritional optimisation is, therefore, a topic that is certainly worthy of further investigation.

## 259 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’ (Dawkins 2008). This definition encompasses the three alternative definitions of animal welfare (Fraser, 2008) 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 (Huntingford et al., 2006), 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 (Eliot et al., 1976; Tsatsoulis and Fountoulakis, 2006). 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 (Schreck and Tort, 2016; Schulte, 2014). 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 (Schreck and Tort, 2016; Schulte, 2014). 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 (Barton and Iwama, 1991; Schreck and Tort, 2016). 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 (Rodnick and Planas, 2016).

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 (Barton et al., 2005; Schreck and Tort, 2016).

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
300 downregulated by chronic stress (Schreck and Tort, 2016). In the striped bass (*Morone saxatilis*), swimming lowered circulating levels of cortisol (Table 2) but did not influence the 301 magnitude of the cortisol response to an acute handling stress (Young and Cech Jr., 1993). In 302 rainbow trout, sustained swimming either lowered (Woodward and Smith, 1985) or did not 303 affect (McKenzie et al., 2012) circulating cortisol titres (Table 2) but, in both studies, there 304 was no significant effect of swimming on the magnitude of the cortisol response to an acute 305 stress. In *matrinxà* (*Brycon amazonicus*), sustained swimming lowered plasma cortisol titres 306 (Arbelaez-Rojas et al., 2017), although it had no effect on their cortisol response to transport 307 stress (Arbeláez-Rojas et al., 2013). Thus, the evidence indicates that swimming has no 308 chronic effects on sensitivity of the HPI axis to acute stress (Table 2.. 309

310 There is strong evidence, however, that providing a current to swim against can 311 accelerate recovery of plasma cortisol homeostasis after acute stresses such as exercise to 312 exhaustion (Milligan et al., 2000), handling (Young and Cech Jr., 1993), confinement 313 (McKenzie et al., 2012; Veiseth et al., 2006) or live transport (Arbelaez-Rojas et al., 2017). 314 Interestingly, the evidence that providing a current promotes more rapid recovery of plasma 315 metabolites following exercise to exhaustion is more mixed. In some studies and species it did 316 (e.g. Lackner et al., 1988; Milligan et al., 2000; Veiseth et al., 2006) whereas, in others, it did 317 not (Kieffer et al., 2011; Meyer and Cook, 1996; Suski et al., 2015). Exercise to exhaustion 318 causes profound metabolic disturbances and should very rarely (or never) occur in 319 aquaculture. The accelerated recovery of cortisol might be a training effect, where fishes that 320 are exercised for extended periods develop greater scope for metabolism, that allows them to 321 recover general homeostasis more rapidly (Lackner et al., 1988; McKenzie et al., 2012). 322

322 To conclude, there is no clear support for the notion that providing a current during 323 rearing can systemically alleviate endocrine 'stress' in fishes. A swimming current may, 324 however, mitigate routine handling and transport stresses, by accelerating recovery of 325 endocrine homeostasis. 326

326 Exercise and immunity

327 There is very limited knowledge regarding the impact of exercise regimes on the immune 328 performance of farmed fishes, but this is an interesting area for research because of the severe 329 impacts that disease can have on aquaculture operations. In mammals, it is now generally 330 accepted that aerobic exercise improves immunocompetency, although intense exhaustive 331 exercise may be immunosuppressive (Campbell and Turner, 2018). In various mammalian
species including humans, exercise influences disease resistance, the capacity to initiate a successful immune response to pathogens, and vaccination success (Pascoe et al., 2014). 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 (Campbell and Turner, 2018).

In fishes, Castro et al. (2013) 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 (Robinson et al., 2017).

In mammals, it is highly likely that cell mobilisation and redistribution throughout the body during exercise significantly contributes to any subsequent changes in tissue immune-related gene expression (Campbell and Turner, 2018). It has proven difficult to understand the tissue distribution of the various cells of the immune response, and their capacity for mobilisation and redistribution (Campbell and Turner, 2018; Hay and Andrade, 1998). 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 (Pascoe et al, 2014). Interestingly, this has been attributed to cytokine release including interleukin-6 (IL-6), and to tissue damage, particularly muscle damage (Bruunsgaard et al., 1997). A recent study in zebrafish (*Danio rerio*) identified increased expression of IL-6 in certain muscle fibres in response to exercise (Rovira et al., 2017). These observations suggest that exercise regimes
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may have potential to increase the effectiveness of vaccination in commercially farmed fish species, by a similar beneficial adjuvant-like effect.

366

**Exercise, cognition and neural plasticity**

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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 (Huntingford and Kadri, 2013). Such effects of exercise are well-established in mammals (Cotman and Berchtold, 2002; van Praag, 2008). In adult rodents, for example, voluntary exercise promotes neurogenesis and expression of neurotrophins, particularly in the hippocampus (Cotman and Berchtold, 2002; Soya et al., 2007). The hippocampus plays an important role in relational memory and spatial orientation (Broglio et al., 2015) and exercised mammals show increased cognitive performance in maze tests compared to sedentary conspecifics (Ma et al., 2017; van Praag, 2008; Vaynman et al., 2004). 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 (Zupanc, 2006; Zupanc and Sîrbulescu, 2011). This fact was a particular stimulus for investigating whether exercise-induced enhancement of neurogenesis and cognition also occurs in fishes (Huntingford and Kadri, 2013).

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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 (Mes et al., 2020). 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 (Mes et al., 2020). 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 (Fiaz et al., 2014). 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.

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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
396 in a conditioning test in zebrafish (Luchiari and Chacon, 2013). However, neither three nor 397 eight weeks of voluntary sustained swimming improved the cognitive performance of Atlantic 398 salmon parr in a maze test, despite increased expression of neuroplasticity markers in their 399 telencephalon (Mes et al., 2018).

400 Overall, the existing findings suggest that, although exercise can promote neural plas-
ticity in teleosts, there is little evidence for an associated increase in cognition. This is an in-
teresting area for future research, in particular with a comprehensive approach that evaluates 401 both neuroplasticity markers and cognitive performance in the same experiment. A particular 402 focus should be upon enhancing cognition in animals that will be used in stocking programs, 403 because hatchery-reared fish are often behaviourally naïve and consequently have low sur- 404 vival rates when released into the wild (Jonsson and Jonsson, 2009; Thorstad et al., 2011). 405 406

407 **Exercise and sexual maturation**

408 Precocious maturation is a significant problem for many important aquaculture species,
409 notably European sea bass (*Dicentrarchus labrax*) (Felip et al., 2008), gilthead seabream
410 (Gines et al., 2003), Atlantic cod (*Gadus morhua*) (Taranger et al., 2006) and Atlantic salmon
411 (Good and Davidson, 2016). As fishes grow, the transition from the juvenile phase,
412 characterised by extensive somatic growth, to a mature adult phase characterized by gonadal
413 recrudescence and spawning, involves a major change in patterns of energy allocation. Energy
414 investments in early maturation may negatively impact growth performance, feed conversion
415 efficiency, fillet quality and the development of the immune system and, consequently, cause
416 important economic losses.

417 Although the exact mechanisms that trigger this transition in energy allocation are still 418 not known, it has been suggested that swimming exercise may play an important role in 419 suppressing sexual maturation. This is because fish species that exhibit lengthy reproductive 420 migrations show delayed or even arrested gonadal development during the migration itself. 421 Such long-distance migrants show swimming-induced suppression of ovarian development at 422 the start of vitellogenesis (or puberty), which may be a strategy to avoid increased drag 423 resistance due to oocyte growth and to prevent precocious muscle atrophy. When female 424 European eels (*Anguilla anguilla*) were subjected to long-term sustained exercise, declines in 425 mRNA expression of estrogen receptor 1, vitellogenin1 and vitellogenin2 in the liver 426 indicated suppression of hepatic vitellogenesis (Palstra et al., 2010a; Palstra and van den 427 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 (Mes et al., 2016). 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. Graziano et al. (2018) 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.
Waldrop et al. (2018) 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 and McKeown, 1989, 1988), exercise can
enhance plasma levels of GH and, in gilthead seabream, it raises plasma IGF-I levels
*(Sánchez-Gurmaches et al., 2013)*. 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 patterns 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 (Jobling et al., 1993).

## 472 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 (Nestor et al., 1996; Rauw et al., 1998). Thus, it has been suggested that the occurrence of cardiac malformations and failures in some lines of farmed salmonids (Mercier et al., 2000; Poppe et al., 2007) 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 (Claireaux et al., 2005). 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 $U_{crit}$ was moderate with large error terms, namely 0.34 ± 0.22 (Blanc and Toulorge, 1981) and 0.24 ± 0.16 (Hurley and Schom, 1984), respectively. Similar heritability estimates of 0.24 ± 0.19 were reported for the guppy *Poecilia reticulata* Peters 1859 (Nicoletto, 1995). 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 (Garenc et al., 1998). In the European sea bass,
heritability of relative maximum burst swimming speed (in BL s⁻¹) was quite high, at 0.55 ±
0.08 (Vandeputte et al., 2016), 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 (Hurley and Schom, 1984) and in European sea bass (0.12; Vandeputte et al., 2016). 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 (Vandeputte et al., 2016). This suggests that the negative relationship between body size and relative swimming speed is purely phenotypic, as has already been established in fishes (Bainbridge, 1958; Beamish, 1978; Bellwood & Fisher, 2001). 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 (Vandeputte et al., 2016). 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 (Jobling et al., 1993; Thorstad et al., 2011).

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.

535

536

537 REFERENCES

538 Alsop, D., Wood, C., 1997. The interactive effects of feeding and exercise on oxygen
539 consumption, swimming performance and protein usage in juvenile rainbow trout
540 (Oncorhynchus mykiss). J. Exp. Biol. 200, 2337-46.

541 Arbeláez-Rojas, G.A., Hackbarth, A., Inoue, L.A.K.A., Dias de Moraes, F., Moraes, G., 2013.

542 Sustained Swimming Mitigates Stress in Juvenile Fish *Brycon amazonicus*. J. Appl.

543 Aquac. 25, 271-281. https://doi.org/10.1080/10454438.2013.817198

544 Arbelaez-Rojas, G.A., Moraes, G., Nunes, C. da S., Fabrizzi, F., 2017. Sustained swimming mitigates stress in juvenile *Brycon amazonicus* reared in high stocking densities. Pesqui.

546 Agropecu. Bras. 52, 1-9. https://doi.org/10.1590/S0100-204X2017000100001

547 Bainbridge, R., 1958. The speed of swimming of fish as related to size and to the frequency
548 and amplitude of the tail beat. J. Exp. Biol. 35, 109-133.

549 Barrett, B.A., McKeown, B.A., 1989. Plasma growth hormone levels in Salmo gairdneri:
550 Studies on temperature and the exercise intensity/duration relationship. Comp. Biochem.

551 Physiol. Part A Physiol. 94, 791-794. https://doi.org/10.1016/0300-9629(89)90635-X

552 Barrett, B.A., McKeown, B.A., 1988. Sustained Exercise Increases Plasma Growth Hormone
553 Concentrations in Two Anadromous Salmonids. Can. J. Fish. Aquat. Sci. 45, 747-749.

554 https://doi.org/10.1139/f88-091

555 Barton, B.A., Iwama, G.K., 1991. Physiological changes in fish from stress in aquaculture
556 with emphasis on the response and effects of corticosteroids. Annu. Rev. Fish Dis. 1, 3-
557 26. https://doi.org/10.1016/0959-8030(91)90019-G

558 Barton, B.A., Ribas, L., Acerete, L., Tort, L., 2005. Effects of chronic confinement on
559 physiological responses of juvenile gilthead sea bream, Sparus aurata L., to acute
560 handling. Aquac. Res. 36, 172-179. https://doi.org/10.1111/j.1365-2109.2004.01202.x

561 Beamish, F.W.H., 1978. Swimming capacity, in: Hoar, W.S., Randall, D.J. (Eds.), Fish
562 Physiology Volume 7. Academic Press, New York, pp. 101-187.

563 Bellwood, D., Fisher, R., 2001. Relative swimming speeds in reef fish larvae. Mar. Ecol.
564 Prog. Ser. 211, 299-303.

565 Blanc, J., Toulorge, J., 1981. Variabilité génétique de la performance de nage chez l'alevin de
566 Truite fario (Salmo trutta). Genet. Sel. Evol. 13, 165. https://doi.org/10.1186/1297-9686-
567 13-2-165

568 Blasco, F.R., Esbaugh, A.J., Killen, S., Rantin, F.T., Taylor, E.W., McKenzie, D.J., 2020.
569 Using aerobic exercise to evaluate sub-lethal tolerance of acute warming in fishes. J.
570 Exp. Biol. 223: jeb218602 doi: 10.1242/jeb.218602

571 Blasco, J., Moya, A., Millán-Cubillo, A., Vélez, E.J., Capilla, E., Pérez-Sánchez, J., Gutiérrez, J., Fernández-Borrás, J., 2015. Growth-promoting effects of sustained swimming in fingerlings of gilthead sea bream (Sparus aurata L.). J. Comp. Physiol. B 185, 859-868.
572
573
574 https://doi.org/10.1007/s00360-015-0933-5

575 Boesgaard, L., Nielsen, M.E., Rosenkilde, P., 1993. Moderate exercise decreases plasma
576 cortisol levels in atlantic salmon (Salmo salar). Comp. Biochem. Physiol. -- Part A
577 Physiol. 106, 641-643. https://doi.org/10.1016/0300-9629(93)90373-C

578 Brett, J.R., 1976. Scope for Metabolism and Growth of Sockeye Salmon, *Oncorhynchus nerka*, and Some Related Energetics. J. Fish. Res. Board Canada 33, 307-313.
579
580 https://doi.org/10.1139/f76-046

581 Brett, J.R., Groves, T.D.D., 1979. Physiological Energetics, in: Hoar, W.S., Randall, D.J.,
582 Brett, J.R. (Eds.), Fish Physiology Volume 8. Academic Press, New York, pp. 280-352.

583 Broglio, C., Martín-Monzón, I., Ocaña, F.M., Gómez, A., Durán, E., Salas, C., Rodríguez, F., 2015. Hippocampal Pallium and Map-Like Memories through Vertebrate Evolution. J. Behav. Brain Sci. 5, 109-120. https://doi.org/10.4236/jbbs.2015.53011

586 Brown, E.J., Bruce, M., Pether, S., Herbert, N.A., 2011. Do swimming fish always grow fast?
587 Investigating the magnitude and physiological basis of exercise-induced growth in
588 juvenile New Zealand yellowtail kingfish, Seriola lalandi. Fish Physiol. Biochem. 37,
589 327–336.

590 Bruunsgaard, H., Galbo, H., Halkjaer-Kristensen, J., Johansen, T.L., MacLean, D.A.,
591 Pedersen, B.K., 1997. Exercise-induced increase in serum interleukin-6 in humans is
592 related to muscle damage. J. Physiol. 499, 833–841.
593 https://doi.org/10.1113/jphysiol.1997.sp021972

594 Burgetz, I., Rojas-Vargas, A., Hinch, S., Randall, D., 1998. Initial recruitment of anaerobic
595 metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). J.
596 Exp. Biol. 201.

597 Cai, L., Fang, M., Johnson, D., Lin, S., Tu, Z., Liu, G., Huang, Y., 2014. Interrelationships
598 between feeding, food deprivation and swimming performance in juvenile grass carp.
599 Aquat. Biol. 20, 69–76. https://doi.org/10.3354/ab00546

600 Campbell, J.P., Turner, J.E., 2018. Debunking the Myth of Exercise-Induced Immune
601 Suppression: Redefining the Impact of Exercise on Immunological Health Across the
602 Lifespan. Front. Immunol. 9, 648. https://doi.org/10.3389/fimmu.2018.00648

603 Castro, V., Grisdale-Helland, B., Helland, S.J., Kristensen, T., Jørgensen, S.M., Helgerud, J.,
604 Claireaux, G., Farrell, A.P., Krasnov, A., Takle, H., 2011. Aerobic training stimulates
605 growth and promotes disease resistance in Atlantic salmon (Salmo salar). Comp.
606 Biochem. Physiol. A. Mol. Integr. Physiol. 160, 278–290.
607 https://doi.org/10.1016/j.cbpa.2011.06.013

608 Castro, V., Grisdale-Helland, B., Jørgensen, S.M., Helgerud, J., Claireaux, G., Farrell, A.P.,
609 Krasnov, A., Helland, S.J., Takle, H., 2013. Disease resistance is related to inherent
610 swimming performance in Atlantic salmon. BMC Physiol. 13, 1.
611 https://doi.org/10.1186/1472-6793-13-1

612 Christiansen, J., Jobling, M., 1990. The behaviour and the relationship between food intake
613 and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained
614 exercise. Can. J. Zool. 68, 2185–2191.

615 Christiansen, J.S., Jørgensen, E.H., Jobling, M., 1991. Oxygen-Consumption in Relation to
616 Sustained Exercise and Social Stress in Arctic Charr (Salvelinus-Alpinus L). J. Exp.
617 Zool. 260, 149–156. https://doi.org/10.1002/jez.1402600203

618 Christiansen, J.S., Ring, E., Jobling, M., 1989. Effects of Sustained Exercise on Growth and
619 Body Composition of First-Feeding Fry of Arctic Charr, Salvelinus alpinus (L.) 79,
620 329-335.

621 Claireaux, G., Couturier, C., Groison, A.-L., 2006. Effect of temperature on maximum
622 swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus
623 labrax). J. Exp. Biol. 209, 3420-8. https://doi.org/10.1242/jeb.02346

624 Claireaux, G., McKenzie, D.J., Genge, a G., Chatelier, A., Aubin, J., Farrell, A.P., 2005.
625 Linking swimming performance, cardiac pumping ability and cardiac anatomy in
626 rainbow trout. J. Exp. Biol. 208, 1775-84. https://doi.org/10.1242/jeb.01587

627 Cotman, C.W., Berchtold, N.C., 2002. Exercise: a behavioral intervention to enhance brain
628 health and plasticity. Trends Neurosci. 25, 295-301. https://doi.org/10.1016/S0166-2236(02)02143-4

630 Davison, W., 1997. The Effects of Exercise Training on Teleost Fish, a Review of Recent
631 Literature 117, 67-75.

632 Davison, W., 1989. Training and its effects on teleost fish. Comp. Biochem. Physiol. Part A
633 Physiol. 94, 1-10. https://doi.org/10.1016/0300-9629(89)90775-5

634 Davison, W., Goldspink, G., 1977. The effect of prolonged exercise on the lateral musculature
635 of the brown trout (Salmo trutta), J. Exp. Biol.

636 Davison, W., Herbert, N.A., 2013. Swimming-Enhanced Growth, in: Swimming Physiology
637 of Fish. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 177-202.
638 https://doi.org/10.1007/978-3-642-31049-2_8

639 Dawkins, M.S., 2008. The Science of Animal Suffering. Ethology 114, 937-945.
640 https://doi.org/10.1111/j.1439-0310.2008.01557.x

641 East, P., Magnan, P., 1987. The effect of locomotor activity on the growth of brook charr,
642 *Salvelinus fontinalis* Mitchill. Can. J. Zool. 65, 843-846. https://doi.org/10.1139/z87-134

643 Eliot, R.S., Forker, A.D., Robertson, R.J., 1976. Aerobic exercise as a therapeutic modality in
644 the relief of stress. Adv. Cardiol. 18, 231-42. https://doi.org/10.1159/000399527

645 Felip, A., Zanuy, S., Muriach, B., Cerdá-Reverter, J.M., Carrillo, M., 2008. Reduction of
646 sexual maturation in male Dicentrarchus labrax by continuous light both before and
647 during gametogenesis. Aquaculture 275, 347-355.
648 https://doi.org/10.1016/J.AQUACULTURE.2008.01.020

649 Felip, O., Blasco, J., Ibarz, A., Martin-Perez, M., Fernández-Borràs, J., 2012. Beneficial
650 effects of sustained activity on the use of dietary protein and carbohydrate traced with
651 stable isotopes 15N and 13C in gilthead sea bream (Sparus aurata). J. Comp. Physiol. B
183, 223-234. https://doi.org/10.1007/s00360-012-0703-6

Felip, O., Ibarz, A., Fernández-Borràs, J., Beltrán, M., Martín-Pérez, M., Planas, J. V., Blasco, J., 2012. Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): Effects of gelatinisation of starches and sustained swimming. Br. J. Nutr. 107, 834-844.

https://doi.org/10.1017/S0007114511003709

Fiaz, A.W., Léon-Kloosterziel, K.M., van Leeuwen, J.L., Kranenbarg, S., 2014. Exploring the effect of exercise on the transcriptome of zebrafish larvae (Danio rerio). J. Appl.

Ichthyol. 30, 728-739. https://doi.org/10.1111/jai.12509

Fitzgibbon, Q.P., Strawbridge, A., Seymour, R.S., 2007. Metabolic scope, swimming performance and the effects of hypoxia in the mulloway, Argyrosomus japonicus (Pisces: Sciaenidae). Aquaculture 270, 358-368.

https://doi.org/10.1016/j.aquaculture.2007.04.038

Forster, I.P., Ogata, H., 1996. Growth and Whole-body Lipid Content of Juvenile Red Sea Bream Reared under Different Conditions of Exercise Training and Dietary Lipid. Fish.

Sci. 62, 404-409. https://doi.org/10.2331/fishsci.62.404

Fraser, D., 2008. Understanding animal welfare. Acta Vet. Scand. 50, S1.

https://doi.org/10.1186/1751-0147-50-S1-S1

Gallaugher, P.E., Thorarensen, H., Kiessling, a, Farrell, A. P., 2001. 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. J. Exp. Biol. 204, 2861-72.

Garenc, C., Silversides, F.G., Guderley, H., 1998. Burst swimming and its enzymatic correlates in the threespine stickleback (Gasterosteus aculeatus): full-sib heritabilities.

Can. J. Zool. 76, 680-688. https://doi.org/10.1139/z97-236

Ghanawi, J., Mohanna, C., Saoud, I.P., 2010. Effect of continuous water movement on growth and body composition of Juvenile rabbitfish, Siganus rivulatus. J. World Aquac. Soc. 41,

834-839. https://doi.org/10.1111/j.1749-7345.2010.00427.x

Gines, R., Afonso, J.M., Arguello, A., Zamorano, M.J., Lopez, J.L., 2003. Growth in adult gilthead sea bream (Sparus aurata L) as a result of interference in sexual maturation by

different photoperiod regimes. Aquac. Res. 34, 73-83. https://doi.org/10.1046/j.1365-2109.2003.00801.x
684 Gonzalez, R.J., McDonald, D.G., 1992. the relationship between oxygen consumption and ion loss in a freshwater fish. J. Exp. Biol. 163.

686 Good, C., Davidson, J., 2016. A Review of Factors Influencing Maturation of Atlantic Salmon, *Salmo salar*, with Focus on Water Recirculation Aquaculture System Environments. J. World Aquac. Soc. 47, 605-632. https://doi.org/10.1111/jwas.12342

689 Graziano, M., Benito, R., Planas, J. V., Palstra, A.P., 2018. Swimming exercise to control precocious maturation in male seabass (Dicentrarchus labrax). BMC Dev. Biol. 18, 10. https://doi.org/10.1186/s12861-018-0170-8

692 Hammer, C., 1995. Fatigue and exercise tests with fish. Comp. Biochem. Physiol. Part A Physiol. 112, 1-20. https://doi.org/10.1016/0300-9629(95)00060-K

694 Hay, J.B., Andrade, W.N., 1998. Lymphocyte recirculation, exercise, and immune responses. Can. J. Physiol. Pharmacol. 76, 490-496. https://doi.org/10.1139/y98-051

696 Houlihan, D.F., Laurent, P., 1987. Effects of Exercise Training on the Performance, Growth, and Protein Turnover of Rainbow Trout (*Salmo gairdneri*). Can. J. Fish. Aquat. Sci. 44, 1614-1621. https://doi.org/10.1139/f87-195

699 Huntingford, F., Kadri, S., 2013. Exercise, Stress and Welfare, in: Palstra, A., Planas, J. (Eds.), Swimming Physiology of Fish. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 161-174. https://doi.org/10.1007/978-3-642-31049-2_7

702 Huntingford, F.A., Adams, C., Braithwaite, V.A., Kadri, S., Pottinger, T.G., Sandoe, P., Turnbull, J.F., 2006. Current issues in fish welfare. J. Fish Biol. 68, 332-372. https://doi.org/10.1111/j.0022-1112.2006.001046.x

705 Hurley, S.M., Schom, C.B., 1984. Genetic control of swimming stamina in Atlantic salmon (*Salmo salar*). Can. J. Genet. Cytol. 26, 57-61. https://doi.org/10.1139/g84-010

707 Ibarz, A., Felip, O., Fernández-Borràs, J., Martín-Pérez, M., Blasco, J., Torrella, J.R., 2011. Sustained swimming improves muscle growth and cellularity in gilthead sea bream. J. Comp. Physiol. B 181, 209-217. https://doi.org/10.1007/s00360-010-0516-4

710 Jobling, M., 2002. Environmental Factors and Rates of Development and Growth, in: Hart, P.J.B., Reynolds, J.D. (Eds.), Handbook of Fish Biology and Fisheries, Volume 1. Blackwell Publishing Ltd, Oxford, pp. 97-122. https://doi.org/10.1002/9780470693803.ch5

714 Jobling, M., Baardvik, B., Christiansen, J., Jorgensen, E., 1993. The effects of prolonged exercise training on growth performance and production parameters in fish. Aquac. Int.
716 1, 95–111.

717 Jonsson, B., Jonsson, N., 2009. Restoration and Enhancement of Salmonid Populations and

718 Habitats with Special Reference to Atlantic Salmon, in: Haro, A., Avery, T., Beal, K.

719 (Eds.), Challenges for Diadromous Fishes in a Dynamic Global Environment, American

720 Fisheries Society Symposium. pp. 497–535.

721 Jørgensen, E.H., Baardvik, B.M., Eliassen, R., Jobling, M., 1996. Food acquisition and

722 growth of juvenile Atlantic salmon (Salmo salar) in relation to spatial distribution of

723 food. Aquaculture 143, 277–289. https://doi.org/10.1016/0044-8486(96)01287-2

724 Jørgensen, E.H., Christiansen, J.S., Jobling, M., 1993. Effects of stocking density on food

725 intake, growth performance and oxygen consumption in Arctic charr (Salvelinus

726 alpinus). Aquaculture 110, 191–204. https://doi.org/10.1016/0044-8486(93)90272-Z

727 Jørgensen, E.H., Jobling, M., 1993. The effects of exercise on growth, food utilisation and

728 osmoregulatory capacity of juvenile Atlantic salmon, Salmo salar. Aquaculture 116, 233–

729 246. https://doi.org/10.1016/0044-8486(93)90011-M

730 Karlsen, O., Norberg, B., Kjesbu, O., Taranger, G., 2006. Effects of photoperiod and exercise

731 on growth, liver size, and age at puberty in farmed Atlantic cod (Gadus morhua L.).

732 ICES J. Mar. Sci. 63, 355–364. https://doi.org/10.1016/j.icesjms.2005.10.013

733 Kaufmann, R., 1990. Respiratory Cost of Swimming in Larval and Juvenile Cyprinids. J. Exp.

734 Biol. 150.

735 Khan, J.R., Trembath, C., Pether, S., Bruce, M., Walker, S.P., Herbert, N.A., 2014.

736 Accommodating the cost of growth and swimming in fishâ€”the applicability of

737 exercise-induced growth to juvenile hapuku (Polyprion oxygeneios). Front. Physiol. 5,

738 448. https://doi.org/10.3389/fphys.2014.00448

739 Kieffer, J., Alsop, D., Wood, C., 1998. A respirometric analysis of fuel use during aerobic

740 swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J. Exp.

741 Biol. 201, 3123–3133.

742 Kieffer, J.D., Kassie, R.S., Taylor, S.G., 2011. The effects of low-speed swimming following

743 exhaustive exercise on metabolic recovery and swimming performance in brook trout

744 (Salvelinus fontinalis). Physiol. Biochem. Zool. 84, 385–393.

745 https://doi.org/10.1086/660891

746 Kiessling, A., Higgs, D.A., Dosanjh, B.S., Eales, J.G., 1994. Influence of Sustained Exercise

747 at Two Ration Levels on Growth and Thyroid Function of All-Female Chinook Salmon (
748 *Oncorhynchus tshawytscha*) in Seawater. Can. J. Fish. Aquat. Sci. 51, 1975-1984.

749 https://doi.org/10.1139/f94-200

750 Kiessling, A., Pickova, J., Eales, J.G., Dosanjh, B., Higgs, D., 2005. Age, ration level, and exercise affect the fatty acid profile of chinook salmon (*Oncorhynchus tshawytscha*) muscle differently. Aquaculture 243, 345-356.

753 https://doi.org/10.1016/J.AQUACULTURE.2004.10.003

754 Lackner, R., Weisler, W., Huber, M., Dalla Via, J., 1988. Responses of the intermediary metabolism to acute handling stress and recovery in untrained and trained Leuciscus Cephalus (Cyprinidae, Teleostei). J. Exp. Biol. 140, 393-404.

757 Larsen, B.K., Skov, P. V., McKenzie, D.J., Jokumsen, A., 2012. The effects of stocking density and low level sustained exercise on the energetic efficiency of rainbow trout (*Oncorhynchus mykiss*) reared at 19°C. Aquaculture 324-325, 226-233.

760 https://doi.org/10.1016/j.aquaculture.2011.10.021

761 Lauff, R.F., Wood, C.M., 1997. Effects of training on respiratory gas exchange, nitrogenous waste excretion, and fuel usage during aerobic swimming in juvenile rainbow trout (*Oncorhynchus mykiss*). Can. J. Fish. Aquat. Sci. 54, 566-571.

764 Lee, C.G., Farrell, A.P., Lotto, A., MacNutt, M.J., Hinch, S.G., Healey, M.C., 2003. The effect of temperature on swimming performance and oxygen consumption in adult sockeye (*Oncorhynchus nerka*) and coho (O. kisutch) salmon stocks. J. Exp. Biol. 206, 3239-3251. https://doi.org/10.1242/jeb.00547

768 Leon, K.A., 1986. Effect of Exercise on Feed Consumption, Growth, Food Conversion, and Stamina of Brook Trout. Progress. Fish-Culturist 48, 43-46.

770 https://doi.org/10.1577/1548-8640(1986)48<43:EOEOFC>2.0.CO;2

771 Li, X.-M., Liu, L., Yuan, J.-M., Xiao, Y.-Y., Fu, S.-J., Zhang, Y.-G., 2016. The effect of aerobic exercise and starvation on growth performance and postprandial metabolic response in juvenile southern catfish (*Silurus meridionalis*). Comp. Biochem. Physiol.

774 Part A Mol. Integr. Physiol. 193, 36-44. https://doi.org/10.1016/J.CBPA.2016.01.007

775 Li, X.M., Yu, L.J., Wang, C., Zeng, L.Q., Cao, Z.D., Fu, S.J., Zhang, Y.G., 2013. The effect of aerobic exercise training on growth performance, digestive enzyme activities and postprandial metabolic response in juvenile qingbo (*Spinibarbus sinensis*). Comp.

778 Biochem. Physiol. - A Mol. Integr. Physiol. 166, 8-16.

779 https://doi.org/10.1016/j.cbpa.2013.04.021
780 Liew, H.J., Sinha, A.K., Mauro, N., Diricx, M., Blust, R., De Boeck, G., 2012. Fasting goldfish, Carassius auratus, and common carp, Cyprinus carpio, use different metabolic strategies when swimming. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 163, 327–335. https://doi.org/10.1016/J.CBPA.2012.07.012

781 Liu, G., Wu, Y., Qin, X., Shi, X., Wang, X., 2018. The effect of aerobic exercise training on growth performance, innate immune response and disease resistance in juvenile Schizothorax prenanti. Aquaculture 486, 18–25. https://doi.org/10.1016/J.AQUACULTURE.2017.12.006

782 Luchiari, A.C., Chacon, D.M.M., 2013. Physical exercise improves learning in zebrafish, Danio rerio. Behav. Processes 100, 44–47. https://doi.org/10.1016/J.BEPROC.2013.07.020

783 Ma, C.-L., Ma, X.-T., Wang, J.-J., Liu, H., Chen, Y.-F., Yang, Y., 2017. Physical exercise induces hippocampal neurogenesis and prevents cognitive decline. Behav. Brain Res. 317, 332–339. https://doi.org/10.1016/J.BBR.2016.09.067

784 Magnoni, L.J., Felip, O., Blasco, J., Planas, J. V., 2013. Metabolic Fuel Utilization During Swimming: Optimizing Nutritional Requirements for Enhanced Performance, in: Swimming Physiology of Fish. Springer Berlin Heidelberg, Berlin, Heidelberg, pp. 203–235. https://doi.org/10.1007/978-3-642-31049-2_9

785 Marras, S., Killen, S.S., Lindström, J., McKenzie, D.J., Steffensen, J.F., Domenici, P., 2015. Fish swimming in schools save energy regardless of their spatial position. Behav. Ecol. Sociobiol. 69, 19–226. https://doi.org/10.1007/s00265-014-1834-4

786 McKenzie, D.J., 2011. Swimming and other activities | Energetics of Fish Swimming, Encyclopedia of Fish Physiology. Elsevier Inc. https://doi.org/10.1016/B978-0-12-374553-8.00151-9

787 McKenzie, D.J., Höglund, E., Dupont-Prinet, a., Larsen, B.K., Skov, P.V., Pedersen, P.B., Jokumsen, a., 2012. Effects of stocking density and sustained aerobic exercise on growth, energetics and welfare of rainbow trout. Aquaculture 338–341, 216–222. https://doi.org/10.1016/j.aquaculture.2012.01.020

788 McKenzie, D.J., Martinez, R., Morales, A., Acosta, J., Morales, R., Taylor, E.W., Steffensen, J.F., Estrada, M.P., 2003. Effects of growth hormone transgenesis on metabolic rate, exercise performance and hypoxia tolerance in tilapia hybrids. J. Fish Biol. 63, 398–409. https://doi.org/10.1046/j.1095-8649.2003.00162.x
812 Mercier, C., Aubin, J., Lefrançois, C., Claireaux, G., 2000. Cardiac disorders in farmed adult brown trout, Salmo trutta L. J. Fish Dis. 23, 243-249. https://doi.org/10.1046/j.1365-2761.2000.00237.x

815 Mes, D., Dirks, R.P., Palstra, A.P., 2016. Simulated migration under mimicked photothermal conditions enhances sexual maturation of farmed European eel (Anguilla anguilla). Aquaculture 452, 367-372. https://doi.org/10.1016/J.AQUACULTURE.2015.11.020

818 Mes, D., Palstra, A., Henkel, C., Vindas, M., Mayer, I., 2018. Brain training: Can swimming exercise promote brain plasticity and cognitive performance in Atlantic salmon?, in: 13th International Congress on the Biology of Fish.

821 Mes, D., Palstra, A.P., Henkel, C. V., Mayer, I., Vindas, M.A., 2020. Swimming exercise enhances brain plasticity in fish. R. Soc. Open Sci. 7, 191640. https://doi.org/10.1098/rsos.191640

824 Meyer, W.F., Cook, P.A., 1996. An assessment of the use of low-level aerobic swimming in promoting recovery from handling stress in rainbow trout. Aquac. Int. 4, 169-174. https://doi.org/10.1007/BF00140597

827 Milligan, C.L., Hooke, G.B., Johnson, C., 2000. Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout. J. Exp. Biol. 203, 921-926. https://doi.org/10.1016/0300-9629(93)90373-c

830 Nestor, K., Noble, D., Zhu, N., Moritsu, Y., 1996. Direct and correlated responses to long-term selection for increased body weight and egg production in turkeys. Poult. Sci. 75, 1180-1191.

833 Nicoletto, P.F., 1995. Offspring quality and female choice in the guppy, Poecilia reticulata. Anim. Behav. 49, 377-387. https://doi.org/10.1006/ANBE.1995.0050

835 Ogata, H.Y., Oku, H., 2000. Effects of Water Velocity on Growth Performance of Juvenile Japanese Flounder Paralichthys olivaceus. J. World Aquac. Soc. 31, 225-231. https://doi.org/10.1111/j.1749-7345.2000.tb00357.x

838 Ohlberger, J., Staaks, G., Hölker, F., 2006. Swimming efficiency and the influence of morphology on swimming costs in fishes. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 176, 17-25. https://doi.org/10.1007/s00360-005-0024-0

841 Palstra, A.P., Crespo, D., van den Thillart, G.E.E.J.M., Planas, J. V., 2010a. Saving energy to fuel exercise: swimming suppresses oocyte development and downregulates ovarian transcriptomic response of rainbow trout *Oncorhynchus mykiss*. Am. J. Physiol. Integr.
844 Comp. Physiol. 299, R486-R499. https://doi.org/10.1152/ajpregu.00109.2010

845 Palstra, A.P., Mes, D., Kusters, K., Roques, J.A.C., Flik, G., Kloet, K., Blonk, R.J.W., 2015.

846 Forced sustained swimming exercise at optimal speed enhances growth of juvenile

847 yellowtail kingfish (Seriola lalandi). Front. Physiol. 5, 506.

848 https://doi.org/10.3389/fphys.2014.00506

849 Palstra, A.P., Planas, J. V., 2013. Swimming physiology of fish: Towards using exercise to farm a fit fish in sustainable aquaculture, Swimming Physiology of Fish: Towards Using

850 Exercise to Farm a Fit Fish in Sustainable Aquaculture. Springer Berlin Heidelberg.

851 https://doi.org/10.1007/978-3-642-31049-2

852 Palstra, A.P., Tudorache, C., Rovira, M., Brittijn, S.A., Burgerhout, E., van den Thillart, G.E.E.J.M., Spaink, H.P., Planas, J. V., 2010b. Establishing zebrafish as a novel exercise

853 model: Swimming economy, swimming-enhanced growth and muscle growth marker gene expression. PLoS One 5. https://doi.org/10.1371/journal.pone.0014483

854 Palstra, A.P., van den Thillart, G.E.E.J.M., 2010. Swimming physiology of European silver eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiol. Biochem. 36, 297-322. https://doi.org/10.1007/s10695-010-9397-4

855 Pascoe, A.R., Fiatarone Singh, M.A., Edwards, K.M., 2014. The effects of exercise on vaccination responses: A review of chronic and acute exercise interventions in humans.

856 Brain. Behav. Immun. 39, 33-41. https://doi.org/10.1016/J.BBI.2013.10.003

857 Peters, C.J., 2009. Continuous Exercise Enhances Swim Performance and Alters Growth Rate, IGF-I, and Cortisol in Juvenile Marine Finfish in Aquaculture. University of San Diego, MSc Thesis.

858 Pettersson, L.B., Hedenström, A., 2000. Energetics, cost reduction and functional consequences of fish morphology. Proc. R. Soc. London. Ser. B Biol. Sci. 267, 759-764.

859 https://doi.org/10.1098/rspb.2000.1068

860 Poppe, T.T., Taksdal, T., Bergtun, P.H., 2007. Suspected myocardial necrosis in farmed Atlantic salmon, Salmo salar L.: a field case. J. Fish Dis. 30, 615-620.

861 https://doi.org/10.1111/j.1365-2761.2007.00841.x

862 Randall, D.J., Baumgarten, D., Malyusz, M., 1972. The relationship between gas and ion transfer across the gills of fishes. Comp. Biochem. Physiol. Part A Physiol. 41, 629-637.

863 https://doi.org/10.1016/0300-9629(72)90017-5
876 Rasmussen, R.S., Heinrich, M.T., Hyldig, G., Jacobsen, C., Jokumsen, A., 2011. Moderate
877 exercise of rainbow trout induces only minor differences in fatty acid profile, texture,
878 white muscle fibres and proximate chemical composition of fillets. Aquaculture 314,
879 159–164. https://doi.org/10.1016/J.AQUACULTURE.2011.02.003

880 Rauw, W., Kanis, E., Noordhuizen-Stassen, E., Grommers, F., 1998. Undesirable side
881 effects of selection for high production efficiency in farm animals: a review. Livest.
882 Prod. Sci. 56, 15–33. https://doi.org/10.1016/S0301-6226(98)00147-X

883 Richards, J.G., Mercado, A.J., Clayton, C. a, Heigenhauser, G.J.F., Wood, C.M., 2002.
884 Substrate utilization during graded aerobic exercise in rainbow trout. J. Exp. Biol. 205,
885 2067–77.

886 Robinson, N.A., Timmerhaus, G., Baranski, M., Andersen, Ø., Takle, H., Krasnov, A., 2017.
887 Training the salmon’s genes: influence of aerobic exercise, swimming performance and
888 selection on gene expression in Atlantic salmon. BMC Genomics 18, 971.
889 https://doi.org/10.1186/s12864-017-4361-7

890 Rodnick, K.J., Planas, J. V., 2016. The Stress and Stress Mitigation Effects of Exercise:
891 Cardiovascular, Metabolic, and Skeletal Muscle Adjustments. Elsevier Inc.
892 https://doi.org/10.1016/B978-0-12-802728-8.00007-2

893 Rovira, M., Arrey, G., Planas, J. V., 2017. Exercise-Induced Hypertrophic and Oxidative
894 Signaling Pathways and Myokine Expression in Fast Muscle of Adult Zebrafish. Front.
895 Physiol. 8, 1063. https://doi.org/10.3389/fphys.2017.01063

896 Sánchez-Gurmaches, J., Cruz-Garcia, L., Ibarz, A., Fernández-Borrás, J., Blasco, J.,
897 Gutiérrez, J., Navarro, I., 2013. Insulin, IGF-I, and muscle MAPK pathway responses
898 after sustained exercise and their contribution to growth and lipid metabolism regulation
899 in gilthead sea bream. Domest. Anim. Endocrinol. 45, 145–153.
900 https://doi.org/10.1016/J.DOMANIEND.2013.08.001

901 Schreck, C.B., Tort, L., 2016. The Concept of Stress in Fish, First Edit. ed, Fish Physiology.
902 Elsevier Inc. https://doi.org/10.1016/B978-0-12-802728-8.00001-1

903 Schulte, P.M., 2014. What is environmental stress? Insights from fish living in a variable
904 environment. J. Exp. Biol. 217, 23–34. https://doi.org/10.1242/jeb.089722

905 Shrivastava, J., Rašković, B., Blust, R., De Boeck, G., 2018. Exercise improves growth, alters
906 physiological performance and gene expression in common carp (Cyprinus carpio).
907 Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 226, 38–48.
908 https://doi.org/10.1016/J.CBPA.2018.08.007

909 Skov, P.V., Larsen, B.K., Frisk, M., Jokumsen, A., 2011. Effects of rearing density and water current on the respiratory physiology and haematology in rainbow trout, Oncorhynchus mykiss at high temperature. Aquaculture 319, 446–452.

912 https://doi.org/10.1016/J.AQUACULTURE.2011.07.008

913 Skov, P. V., Lund, I., Pargana, A.M., 2015. No evidence for a bioenergetic advantage from forced swimming in rainbow trout under a restrictive feeding regime. Front. Physiol. 6, 31. https://doi.org/10.3389/fphys.2015.00031

916 Soya, H., Nakamura, T., Deocaris, C.C., Kimpara, A., Iimura, M., Fujikawa, T., Chang, H., McEwen, B.S., Nishijima, T., 2007. BDNF induction with mild exercise in the rat hippocampus. Biochem. Biophys. Res. Commun. 358, 961–967.

919 https://doi.org/10.1016/J.BBRC.2007.04.173

920 Steffensen, J.F., 1985. The Transition between Branchial Pumping and Ram Ventilation in Fishes: Energetic Consequences and Dependence on Water Oxygen Tension. J. Exp. Biol. 114.

923 Steinhausen, M.F., Fleng Steffensen, J., Gerner Andersen, N., 2010. The effects of swimming pattern on the energy use of gilthead seabream (*Sparus aurata* L.). Mar. Freshw. Behav. Physiol. 43, 227–241. https://doi.org/10.1080/10236244.2010.501135

926 Suski, C.D., Cooke, S.J., Tufts, B.L., 2015. Failure of low-velocity swimming to enhance recovery from exhaustive exercise in largemouth bass (Micropterus salmoides). Physiol. Biochem. Zool. 80, 78–87. https://doi.org/10.1086/509058

929 Taranger, G., Aardal, L., Hansen, T., Kjesbu, O., 2006. Continuous light delays sexual maturation and increases growth of Atlantic cod (Gadus morhua L.) in sea cages. ICES J. Mar. Sci. 63, 365–375. https://doi.org/10.1016/j.icesjms.2005.10.014

932 Thorstad, E.B., Uglem, I., Arechavala-Lopez, P., Økland, F., Finstad, B., 2011. Low survival of hatchery-released A Atlantic salmon smolts during initial river and fjord migration. Boreal Environ. Res. 16, 115–120.

935 Totland, G.K., Kryvi, H., Jødestøl, K.A., Christiansen, E.N., Tangerås, A., Slinde, E., 1987. Growth and composition of the swimming muscle of adult Atlantic salmon (Salmo salar L.) during long-term sustained swimming. Aquaculture 66, 299–313.

938 https://doi.org/10.1016/0044-8486(87)90115-3

939 Tsatsoulis, A., Fountoulakis, S., 2006. The protective role of exercise on stress system
940 dysregulation and comorbidities. Ann. N. Y. Acad. Sci. 1083, 196–213.

941 https://doi.org/10.1196/annals.1367.020

942 Tucker, V.A., 1970. Energetic cost of locomotion in animals. Comp. Biochem. Physiol. 34, 841–846.

944 Tudorache, C., O’Keefe, R.A., Benfey, T.J., 2011. Optimal swimming speeds reflect preferred swimming speeds of brook charr (Salvelinus fontinalis Mitchill, 1874). Fish Physiol. Biochem. 37, 307–315. https://doi.org/10.1007/s10695-011-9498-8

947 van Praag, H., 2008. Neurogenesis and Exercise: Past and Future Directions. NeuroMolecular Med. 10, 128–140. https://doi.org/10.1007/s12017-008-8028-z

949 Vandeputte, M., Porte, J.D., Auperin, B., Dupont-Nivet, M., Vergnet, A., Valotaire, C., Claireaux, G., Prunet, P., Chatain, B., 2016. Quantitative genetic variation for post-stress cortisol and swimming performance in growth-selected and control populations of European sea bass (Dicentrarchus labrax). Aquaculture 455, 1–7. https://doi.org/10.1016/j.AQUACULTURE.2016.01.003

954 Vaynman, S., Ying, Z., Gomez-Pinilla, F., 2004. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur. J. Neurosci. 20, 2580–2590. https://doi.org/10.1111/j.1460-9568.2004.03720.x

957 Veiseth, E., Fjaera, S.O., Bjerkeng, B., Skjervold, P.O., 2006. Accelerated recovery of Atlantic salmon (Salmo salar) from effects of crowding by swimming. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 144, 351–8. https://doi.org/10.1016/j.cbpb.2006.03.009

960 Videler, J.J., 1993. Fish Swimming. Chapman and Hall, London.

961 Waldrop, T., Summerfelt, S., Mazik, P., Good, C., 2018. The effects of swimming exercise and dissolved oxygen on growth performance, fin condition and precocious maturation of early-rearing Atlantic salmon *Salmo salar*. Aquac. Res. 49, 801–808. https://doi.org/10.1111/are.13511

965 Webb, P.W., 1998. Swimming, in: Evans, D.D. (Ed.), The Physiology of Fishes. CRC Press, Boca Raton, pp. 1–38.

967 Weihs, D., Keyes, R.S., Stalls, D.M., 1981. Voluntary Swimming Speeds of Two Species of Large Carcharhinid Sharks. Copeia 1981, 219. https://doi.org/10.2307/1444062

969 Wilson, R.O.D.W., Egginton, S., 1994. Assessment of maximum sustainable swimming performance in rainbow trout (Oncorhynchus mykiss) 305, 299–305.

971 Woodward, J., Smith, L., 1985. Exercise training and the stress response in rainbow trout,
972 Salmo gairdneri Richardson. J. Fish Biol. 26, 435-447.

973 Yogata, H., Oku, H., 2000. The effects of swimming exercise on growth and whole-body

974 protein and fat contents of fed and unfed fingerling yellowtail. Fish. Sci. 66, 1100-1105.

975 Young, P.S., Cech Jr., J.J., 1993. Effects of Exercise Conditioning on Stress Responses and

976 Recovery in Cultured and Wild Young-of-the-Year Striped Bass, Morone saxatilis. Can.

977 J. Fish. Aquat. Sci. 50, 2094-2099. https://doi.org/10.1139/f93-233

978 Zupanc, G.K.H., 2006. Neurogenesis and neuronal regeneration in the adult fish brain. J.

979 Comp. Physiol. A 192, 649-670. https://doi.org/10.1007/s00359-006-0104-y

980 Zupanc, G.K.H., Sîrbulescu, R.F., 2011. Adult neurogenesis and neuronal regeneration in the

981 central nervous system of teleost fish. Eur. J. Neurosci. 34, 917-929.

982 https://doi.org/10.1111/j.1460-9568.2011.07854.x

983
984 **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 (L<sub>i</sub>, 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

<table><thead><tr><th>Species</th><th>Order,<br>Family</th><th>BM<sub>i</sub><br>(g)</th><th>BM<sub>F</sub><br>(g)</th><th>L<sub>i</sub><br>(mm)</th><th>U<br>(BL s<sup>-1</sup>)</th><th>Tank</th><th>T<br>(°C)</th><th>FI<br>(g day<sup>-1</sup>)</th><th>FP</th><th>FCR</th><th>SGR<br>(g day<sup>-1</sup>)</th><th>Reference</th></tr></thead><tbody><tr><td rowspan="5"><i>Sparus aurata</i></td><td rowspan="5">Sparidae</td><td>88±1</td><td>98±2</td><td>0</td><td>200C</td><td>20</td><td>2.6</td><td>AL</td><td></td><td>0.61</td><td rowspan="2">(Ibarz et al., 2011)</td></tr><tr><td>90±1</td><td>107±2</td><td>1.5</td><td>400C</td><td>20</td><td>2.8</td><td>AL</td><td></td><td>0.76</td></tr><tr><td>5.0±0.1</td><td>14.5±0.5</td><td>0</td><td>200C</td><td>23</td><td></td><td>AL</td><td>1.17</td><td>3.41</td><td rowspan="2">(Blasco et al., 2015)</td></tr><tr><td>5.1±0.2</td><td>20.3±0.4</td><td>5</td><td>400C</td><td>23</td><td></td><td>AL</td><td>0.93</td><td>3.72</td></tr><tr><td>50-60</td><td>70±2</td><td>0</td><td>200C</td><td>22</td><td>3.56±0.20</td><td>AL</td><td></td><td>1.13±0.05</td><td>(Felip et al., 2012)</td></tr><tr><td rowspan="6"><i>Pagrus major</i></td><td rowspan="6">Sparidae</td><td>50-60</td><td>74±2</td><td>1.5</td><td>400C</td><td>22</td><td>3.84±0.03</td><td>AL</td><td></td><td>1.32±0.06</td><td rowspan="6">(Forster and Ogata, 1996)</td></tr><tr><td>2.5±0.5</td><td>13.8</td><td>0</td><td>35C</td><td>27.5</td><td>3.16</td><td>AL ×2</td><td>0.81</td><td>4.4</td></tr><tr><td>2.5±0.5</td><td>13.8</td><td>1.5</td><td>35C</td><td>27.5</td><td>3.16</td><td>AL ×2</td><td>0.83</td><td>4.5</td></tr><tr><td>2.5±0.5</td><td>12.7</td><td>3.0</td><td>35C</td><td>27.5</td><td>2.92</td><td>AL ×2</td><td>0.79</td><td>4.2</td></tr><tr><td>2.5±0.5</td><td>14.7</td><td>0</td><td>35C</td><td>27.5</td><td>3.25</td><td>AL ×2</td><td>0.81</td><td>4.6</td></tr><tr><td>2.5±0.5</td><td>15.2</td><td>1.5</td><td>35C</td><td>27.5</td><td>3.03</td><td>AL ×2</td><td>0.75</td><td>4.6</td></tr><tr><td></td><td>2.5±0.5</td><td>12.2</td><td>3.0</td><td>35C</td><td>27.5</td><td>3.40</td><td>AL ×2</td><td>0.94</td><td>4.1</td></tr></tbody></table>
<table><tr><td></td><td></td><td>18±1</td><td>27.3</td><td>0</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.27</td><td>1.56</td></tr><tr><td></td><td></td><td>18±1</td><td>25.8</td><td>1</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.43</td><td>1.39</td></tr><tr><td></td><td></td><td>18±1</td><td>26.7</td><td>2</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.47</td><td>1.42</td></tr><tr><td></td><td></td><td>18±1</td><td>27.5</td><td>0</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.20</td><td>1.62</td></tr><tr><td></td><td></td><td>18±1</td><td>27.0</td><td>1</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.39</td><td>1.44</td></tr><tr><td></td><td></td><td>18±1</td><td>26.4</td><td>2</td><td>35C</td><td>25</td><td>2.5</td><td>RE</td><td>1.45</td><td>1.37</td></tr></table>

<table><tr><td rowspan="5">Seriola<br>quinqueradi<br>ata</td><td rowspan="5">Carangidae</td><td>4.3±0.1</td><td>22.8±0.8</td><td>73</td><td>0.3</td><td>40C</td><td>23</td><td>4.44</td><td>AL ×2</td><td>0.71</td><td>6.03</td></tr><tr><td>4.3±0.1</td><td>30.5±1.7</td><td>73</td><td>1.0</td><td>40C</td><td>23</td><td>4.30</td><td>AL ×2</td><td>0.63</td><td>7.00</td></tr><tr><td>4.4±0.02</td><td>30.5±1.1</td><td>73</td><td>2.25</td><td>40C</td><td>23</td><td>4.21</td><td>AL ×2</td><td>0.62</td><td>6.94</td></tr><tr><td>4.4±0.1</td><td>25.1±0.9</td><td>74</td><td>0.3</td><td>40C</td><td>23</td><td>4.36</td><td>AL ×2</td><td>0.68</td><td>6.23</td></tr><tr><td>4.3±0.1</td><td>29.9±0.7</td><td>73</td><td>1.0</td><td>40C</td><td>23</td><td>4.27</td><td>AL ×2</td><td>0.62</td><td>6.92</td></tr></table>

<table><tr><td rowspan="2">Seriola<br>lalandi</td><td rowspan="2">Carangidae</td><td>504±27</td><td>661±32</td><td>346</td><td>0.0</td><td>3600F</td><td>23.6</td><td>2.65</td><td>RE ×2</td><td>1.77</td><td>1.5</td></tr><tr><td>504±27</td><td>735±23</td><td>346</td><td>2.46</td><td>3600F</td><td>23.6</td><td>2.65</td><td>RE ×2</td><td>1.21</td><td>2.1</td></tr></table>

<table><tr><td rowspan="6">Seriola<br>lalandi</td><td rowspan="6">Carangidae</td><td>1591±7</td><td></td><td>476</td><td>0.0</td><td>13000C</td><td>14.9</td><td></td><td>AL ×2</td><td>2.39</td><td>0.42</td></tr><tr><td>1591±7</td><td></td><td>476</td><td>0.75</td><td>13000C</td><td>14.9</td><td></td><td>AL ×2</td><td>2.18</td><td>0.4</td></tr><tr><td>179±5</td><td></td><td>236</td><td>0.0</td><td>1000C</td><td>21.1</td><td></td><td>AL ×2</td><td>2.05</td><td>0.8</td></tr><tr><td>179±5</td><td></td><td>236</td><td>0.75</td><td>1000C</td><td>21.1</td><td></td><td>AL ×2</td><td>1.89</td><td>0.88</td></tr><tr><td>179±5</td><td></td><td>236</td><td>1.54</td><td>1000C</td><td>21.1</td><td></td><td>AL ×2</td><td>1.93</td><td>0.86</td></tr><tr><td>179±5</td><td></td><td>236</td><td>2.25</td><td>1000C</td><td>21.1</td><td></td><td>AL ×2</td><td>1.98</td><td>0.82</td></tr></table>

<table><tr><td rowspan="2">Siganus<br>rivulatus</td><td rowspan="2">Siganidae</td><td>7.0±0.2</td><td>15.4±0.5</td><td>89</td><td>0.0</td><td>1000C</td><td>26</td><td>3.0</td><td>RE ×2</td><td>1.3</td><td>2.13</td></tr><tr><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td><td></td></tr></table>

(Yogata and Oku, 2000)

(Palstra et al., 2015)

(Brown et al., 2011)

(Ghanawi et al., 2010)
<table><tbody><tr><td></td><td></td><td>7.6±0.2</td><td>13.7±0.4</td><td>91</td><td>1.5</td><td>1000C</td><td>26</td><td>3.0</td><td>RE×2</td><td>1.8</td><td>1.6</td><td></td></tr><tr><td rowspan="15">Polyprion oxygeneios</td><td rowspan="15">Polyprionidae</td><td>120±3</td><td>341±10</td><td></td><td>0.0</td><td>1600C</td><td>17</td><td>218*</td><td>AL×2</td><td>0.97</td><td>1.81</td><td rowspan="15">(Khan et al., 2014)</td></tr><tr><td>131±5</td><td>367±10</td><td></td><td>0.25</td><td>1600C</td><td>17</td><td>227*</td><td>AL×2</td><td>0.97</td><td>1.85</td></tr><tr><td>129±5</td><td>381±13</td><td></td><td>0.5</td><td>1600C</td><td>17</td><td>236*</td><td>AL×2</td><td>0.97</td><td>1.88</td></tr><tr><td>123±5</td><td>365±12</td><td></td><td>0.75</td><td>1600C</td><td>17</td><td>243*</td><td>AL×2</td><td>0.99</td><td>1.88</td></tr><tr><td>133±4</td><td>376±7</td><td></td><td>1.0</td><td>1600C</td><td>17</td><td>249*</td><td>AL×2</td><td>1.01</td><td>1.86</td></tr><tr><td>139±3</td><td>3812±8</td><td></td><td>1.5</td><td>1600C</td><td>17</td><td>258*</td><td>AL×2</td><td>1.07</td><td>1.77</td></tr><tr><td>170±6</td><td>383±12</td><td></td><td>0.0</td><td>1600C</td><td>17</td><td>210*</td><td>AL×2</td><td>1.01</td><td>1.40</td></tr><tr><td>170±8</td><td>373±6</td><td></td><td>0.25</td><td>1600C</td><td>17</td><td>220*</td><td>AL×2</td><td>1.01</td><td>1.43</td></tr><tr><td>171±6</td><td>397±14</td><td></td><td>0.5</td><td>1600C</td><td>17</td><td>227*</td><td>AL×2</td><td>1.01</td><td>1.44</td></tr><tr><td>187±11</td><td>424±20</td><td></td><td>0.75</td><td>1600C</td><td>17</td><td>230*</td><td>AL×2</td><td>1.02</td><td>1.45</td></tr><tr><td>172±10</td><td>388±19</td><td></td><td>1.0</td><td>1600C</td><td>17</td><td>229*</td><td>AL×2</td><td>1.03</td><td>1.44</td></tr><tr><td>167±6</td><td>372±6</td><td></td><td>1.5</td><td>1600C</td><td>17</td><td>218*</td><td>AL×2</td><td>1.07</td><td>1.40</td></tr><tr><td colspan="12">Gadiformes</td></tr><tr><td rowspan="2">Gadus morhua</td><td rowspan="2">Gadidae</td><td>551</td><td>2200</td><td></td><td>0.5 -1.0</td><td>7000C</td><td>7</td><td></td><td>AL×2</td><td></td><td></td><td rowspan="2">(Karlsen et al., 2006)</td></tr><tr><td>450</td><td>2300</td><td></td><td>0.5 - 1.0</td><td>7000C</td><td>10</td><td></td><td>AL×2</td><td></td><td></td></tr><tr><td colspan="12">Pleuronectiforme</td></tr><tr><td rowspan="3">Paralichthys olicaceus</td><td rowspan="3">Paralichthyidae</td><td>5.7 ± 0.1</td><td>41.5 ± 1.3</td><td>91</td><td>0.3</td><td>35C</td><td>21</td><td>1.71</td><td>AL×2</td><td>0.64</td><td>3.35</td><td rowspan="3">(Ogata and Oku, 2000)</td></tr><tr><td>5.8 ± 0.1</td><td>44.8 ± 1.0</td><td>92</td><td>0.9</td><td>35C</td><td>21</td><td>1.75</td><td>AL×2</td><td>0.64</td><td>3.45</td></tr><tr><td>5.7 ± 0.0</td><td>37.7 ± 1.3</td><td>91</td><td>2.1</td><td>35C</td><td>21</td><td>1.72</td><td>AL×2</td><td>0.68</td><td>3.14</td></tr><tr><td colspan="12">Siluriformes</td></tr></tbody></table>
<table><tbody><tr><td rowspan="3">Silurus meridionalis</td><td rowspan="3">Siluridae</td><td>12.2±0.1</td><td>37.1±1.2</td><td>0</td><td>42F</td><td>25</td><td>5.8</td><td>AL ×1</td><td>2.09±0.12</td><td rowspan="3">(Li et al., 2016)</td></tr><tr><td>12.0±0.1</td><td>35.7±0.9</td><td>1</td><td>42F</td><td>25</td><td>6.0</td><td>AL ×1</td><td>3.11</td></tr><tr><td>12.2±0.1</td><td>34.7±1.1</td><td>2</td><td>42F</td><td>25</td><td>6.4</td><td>AL ×1</td><td>3.46</td></tr><tr><td rowspan="4">Schizothorax prenanti</td><td rowspan="4">Cypriniformes Cyprinidae</td><td>13.8±0.1</td><td>24.4±1.4</td><td>0</td><td>1200F</td><td></td><td>17.3±1.7*</td><td>AL ×2</td><td>1.64</td><td>0.95±0.08</td><td rowspan="4">(Liu et al., 2018)</td></tr><tr><td>13.8±0.2</td><td>29.7±1.4</td><td>1</td><td>1200F</td><td></td><td>23.0±1.0*</td><td>AL ×2</td><td>1.45</td><td>1.28±0.07</td></tr><tr><td>13.8±0.2</td><td>31.2±1.4</td><td>2</td><td>1200F</td><td></td><td>24.3±1.2*</td><td>AL ×2</td><td>1.45</td><td>1.36±0.05</td></tr><tr><td>13.8±0.2</td><td>26.4±1.0</td><td>4</td><td>1200F</td><td></td><td>26.5±1.1*</td><td>AL ×2</td><td>2.13</td><td>1.08±0.05</td></tr><tr><td rowspan="4">Spinibarbus sinensis</td><td rowspan="4">Cyprinidae</td><td>19.4±0.1</td><td>40.8±0.8</td><td>102</td><td>0</td><td>42F</td><td>25</td><td>1.63±0.03</td><td>AL ×2</td><td>1.29</td><td>1.32</td><td rowspan="4">(Li et al., 2013)</td></tr><tr><td>19.4±0.1</td><td>49.4±2.2</td><td>102</td><td>1</td><td>42F</td><td>25</td><td>1.94±0.05</td><td>AL ×2</td><td>1.25</td><td>1.66</td></tr><tr><td>19.6±0.1</td><td>53.3±3.4</td><td>103</td><td>2</td><td>42F</td><td>25</td><td>2.05±0.04</td><td>AL ×2</td><td>1.25</td><td>1.79</td></tr><tr><td>19.6±0.1</td><td>47.4±2.0</td><td>103</td><td>3</td><td>42F</td><td>25</td><td>2.22±0.01</td><td>AL ×2</td><td>1.50</td><td>1.58</td></tr></tbody></table>

988 BL, bodylength s⁻¹; C, circular; F, flume; AL, *ad-libitum*; RE, restricted; FCR calculated as feed mass/body mass gain.

989

990
<table><caption>Table 2. Studies that have investigated effects of chronic (days to months) sustained swimming exercise on circulating levels of cortisol in fishes.</caption><thead><tr><th>Species</th><th>Mass (g)</th><th>Forklength (mm)</th><th>Current speed (BL s<sup>-1</sup>)</th><th>Density (kg m<sup>-3</sup>)</th><th>Duration (days)</th><th>Plasma cortisol (ng ml<sup>-1</sup>)</th><th>Reference</th></tr></thead><tbody><tr><td colspan="8"><strong>Decreased plasma cortisol</strong></td></tr><tr><td>Oncorhynchus mykiss</td><td>28</td><td>120</td><td>0.0</td><td>43</td><td>30</td><td>83</td><td>(Woodward and Smith, 1985)</td></tr><tr><td></td><td>29</td><td></td><td>1.5</td><td>43</td><td></td><td>41*</td><td></td></tr><tr><td>Salmo salar</td><td>20</td><td>130</td><td>0.0<br>0.5</td><td>1.7</td><td>4</td><td></td><td>(Boesgaard et al., 1993)</td></tr><tr><td>Morone saxatilis</td><td>23</td><td></td><td>0.0</td><td>5-6</td><td>60</td><td>27</td><td>(Young and Cech Jr., 1993)</td></tr><tr><td></td><td>26</td><td></td><td>0.5-1.2</td><td>5-6</td><td></td><td>19</td><td></td></tr><tr><td></td><td>27</td><td></td><td>1.5-2.4</td><td>5-6</td><td></td><td>3*</td><td></td></tr><tr><td></td><td>26</td><td></td><td>2.4-3.6</td><td>5-6</td><td></td><td>13</td><td></td></tr><tr><td>Brycon amazonicus</td><td>18</td><td>120</td><td>0.0</td><td>1.63</td><td>70</td><td></td><td>(Arbeláez-Rojas et al., 2013)</td></tr><tr><td></td><td></td><td></td><td></td><td>3.26<br>6.53</td><td></td><td></td><td></td></tr><tr><td></td><td></td><td></td><td>1.0</td><td>1.63<br>3.26<br>6.53</td><td></td><td></td><td></td></tr></tbody></table>
<table><thead><tr><th colspan="8">No effect on plasma cortisol</th></tr></thead><tbody><tr><td rowspan="4">O. mykiss</td><td>242</td><td></td><td>0.0</td><td>25</td><td>60</td><td>1</td><td>(McKenzie et al., 2012)</td></tr><tr><td>236</td><td></td><td>0.9</td><td></td><td></td><td>1</td><td></td></tr><tr><td>223</td><td></td><td>0.0</td><td>100</td><td></td><td>&lt;1</td><td></td></tr><tr><td>224</td><td></td><td>0.9</td><td></td><td></td><td>&lt;1</td><td></td></tr><tr><td rowspan="3">Atractoscion nobilis</td><td rowspan="3">42</td><td rowspan="3">108</td><td>0.0</td><td rowspan="3">6.9</td><td rowspan="3">42</td><td rowspan="3"></td><td rowspan="3">(Peters, 2009)</td></tr><tr><td>1.3</td></tr><tr><td>2.0</td></tr><tr><td rowspan="3">Seriola lalandi</td><td rowspan="3">34</td><td rowspan="3">84</td><td>0.0</td><td rowspan="3">7.6</td><td rowspan="3">34</td><td rowspan="3"></td><td rowspan="3">(Peters, 2009)</td></tr><tr><td>1.4</td></tr><tr><td>2.1</td></tr><tr><td colspan="8">Increased plasma cortisol</td></tr><tr><td rowspan="2">Salvelinus alpinus</td><td>102</td><td>196</td><td>0.0</td><td>17-19</td><td>76</td><td>24</td><td>(Christiansen et al., 1991)</td></tr><tr><td>106</td><td>198</td><td>1.3</td><td></td><td></td><td>40*</td><td></td></tr></tbody></table>
994 **Figure legends**

995 **Figure 1.** a) Schematic picture showing different components of metabolic rate in fishes as
996 swimming speed increases up to $U_{ms}$ (maximum sustained swimming speed). The standard
997 metabolic rate (SMR, the basal metabolic rate of ectothermic species at their acclimation
998 temperature), is assumed to be constant at all swimming velocities. The cost of swimming
999 increases exponentially with swimming velocity and the curve is derived from Webb (1971).

1000 The specific dynamic action (SDA, the metabolic cost of digesting and assimilating a meal) is
1001 assumed to be maintained at all swimming velocities (Alsop & Wood, 1997; Thorarensen &
1002 Farrell, 2006). b) The Cost of Transportation (COT, the energy consumed while swimming
1003 one metre) is calculated based on the values in Fig 1a.

1004 **Figure 2.** A conceptual model of the interplay among metabolic rate, feed intake and scope
1005 for growth in fish. At low velocities feed intake ① may or may not be reduced, and/or
1006 metabolic rate increased ②, due to increased levels of spontaneous activity or aggression. As
1007 a result, the scope for growth is reduced. If neither feed intake is reduced nor metabolic rate
1008 increased, scope for growth is maintained over different swimming velocities and there is no
1009 effect of swimming exercise on growth. At swimming velocities above 45-50% of the
1010 maximum sustained swimming speed ($U_{ms}$) growth is reduced because feed intake cannot
1011 meet the increased metabolic demands of swimming, and/or because feed intake is reduced
1012 ③.

1013
<figure><img src="image_2.png" /></figure>
<figure><img src="image_3.png" /></figure>