reviewpaper … · 1950 j. i. johnssonet al. experienced environment p henot y pe n h n (a) h (c) n...

Journal of Fish Biology (2014) 85, 1946–1971

doi:10.1111/jfb.12547, available online at wileyonlinelibrary.com

REVIEW PAPER

Environmental effects on behavioural developmentconsequences for fitness of captive-reared fishes in the wild

J. I. Johnsson*†, S. Brockmark‡ and J. Näslund*

*University of Gothenburg, Department of Biological and Environmental Sciences, Box 463,SE 405 30 Gothenburg, Sweden and ‡Swedish Agency for Sea and Water Management, Box

11 930, SE-404 39 Gothenburg, Sweden

Why do captive-reared fishes generally have lower fitness in natural environments than wild con-specifics, even when the hatchery fishes are derived from wild parents from the local population?A thorough understanding of this question is the key to design artificial rearing environments thatoptimize post-release performance, as well as to recognize the limitations of what can be achievedby modifying hatchery rearing methods. Fishes are generally very plastic in their development andthrough gene–environment interactions, epigenetic and maternal effects their phenotypes will developdifferently depending on their rearing environment. This suggests that there is scope for modifying con-ventional rearing environments to better prepare fishes for release into the wild. The complexity of thenatural environment is impossible to mimic in full-scale rearing facilities. So, in reality, the challenge isto identify key modifications of the artificial rearing environment that are practically and economicallyfeasible and that efficiently promote development towards a more wild-like phenotype. Do such keymodifications really exist? Here, attempts to use physical enrichment and density reduction to improvethe performance of hatchery fishes are discussed and evaluated. These manipulations show potentialto increase the fitness of hatchery fishes released into natural environments, but the success is stronglydependent on adequately adapting methods to species and life stage-specific conditions.

© 2014 The Fisheries Society of the British Isles

Key words: density; hatchery; phenotypic variation; physical structure; reaction norm; salmonids.

‘Our success in repopulating our rivers with species indigenous to themand in acclimating in new waters species which are valuable for food orsport, will be measured by the fidelity and precision with which we study,interpret and apply the lessons taught us by the naturalist, the biologist,the physicist and the chemist.’

M. M’Donald, 1885

INTRODUCTION

T H E A I M O F T H I S PA P E R A N D W H AT I T D O E S N OT C OV E R

This paper summarizes and discusses results from recent research highlighting thepossibilities as well as the challenges associated with improving the post-release

†Author to whom correspondence should be addressed. Tel.: +46 31 7863665; email: [email protected]

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© 2014 The Fisheries Society of the British Isles

B E H AV I O U R A N D F I T N E S S O F C A P T I V E- R E A R E D F I S H E S 1947

performance of captive-reared fishes by environmental modification of the captiveenvironment. Here, welfare (Browman & Skiftesvik, 2007) will not be discussed indepth. It is enough to stress that fishes show an incredible diversity of adaptations andwhere new studies are accumulating evidence of a level of cognitive ability, learningcapacity and environmental sensitivity that was unheard of not many years ago (Brownet al., 2011). The primary focus is on environmental effects and gene–environmentinteractions on hatchery-reared offspring of wild parents. Multi-generational geneticeffects of domestication and artificial selection are very important aspects to under-stand long-term consequences of stocking and potential effects on wild populations,but will not be the main focus here. These aspects have been thoroughly addressedin a number of recent studies which are highly recommended (Fleming et al., 2000;McGinnity et al., 2003; Araki et al., 2007; Berejikian et al., 2009; Lorenzen et al.,2012; Neely et al., 2012; Skaala et al., 2012; Baskett & Waples, 2013; Pulcini et al.,2013).

It should be stressed that habitat restoration should always be the first choice in fishconservation efforts, and hatchery releases should only be considered in cases wherethere are no other realistic ways to save or maintain sensitive natural populations(Einum & Fleming, 2001; Araki et al., 2007). While it is naive to believe that wild andhatchery fishes could ever be ecologically exchangeable (Bisson et al., 2000; Brannonet al., 2004), hatchery rearing methods for conservation and supplementation are,despite a long history, still in their infancy and could potentially be developed to pro-duce fishes more suited for life in the wild (Wiley et al., 1993; Salvanes & Braithwaite,2006; Le Vay et al., 2007: Lorenzen et al., 2010). Considering the spatial and temporalvariation of innumerable biotic and abiotic factors in natural environments, e.g. rivers,and the complex interactions among these factors (Fig. 1; Giller & Malmqvist, 1998;Huntingford et al., 2012): Is it feasible to try to mimic any key aspects of these naturalconditions in a full-scale hatchery to produce fishes better adapted to the wild? Couldbehavioural studies in artificial environments, such as aquaria or hatchery tanks,provide information about how fishes will perform in the wild?

H AT C H E RY E F F E C T S O N B E H AV I O U R : A N O L D P RO B L E M

Artificial rearing of fishes for stocking has a long history (Goode, 1881; Kerr, 2006).According to Goode (1881), the art of fish culture was invented by Stephan LudwigJacobi in Germany in the mid-18th century, an achievement for which he was rewardedlife pension by King George III of the U. K. Since then, artificially propagated fisheshave been stocked in large numbers in streams, rivers, ponds, lakes and the sea at var-ious stages of development. Originally, these activities were mainly intended to boostthe yield of fishes in stocked waters. Early on, however, fishery managers were awareof behavioural changes induced by artificial rearing environments. For example, at afishery management meeting held on 17 March 1919 in Stockholm the Swedish fisheryinstructor Sörensen (1919) stated (free translation from Swedish): ‘These fish [Atlanticsalmon] have become so tame that they are unsuitable to persist in the struggle for sur-vival as it is manifested in nature, including the water [… ] their innate natural cautionis completely vanished. If you hold a net just below the water surface and throw somefood over it, the fish gather in a school around the food.[… ] this as an example of howthe shyness of the fish, by which it avoids many dangers, disappears during regularfeeding’.

© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971

1948 J . I . J O H N S S O N E T A L.

Turbid Clear

Water level

Water level

(a)

(b)

Fig. 1. Some key environmental differences between a (a) natural stream and (b) conventional hatchery environ-ment that are likely to affect phenotypic development (Giller & Malmqvist, 1998; Huntingford et al., 2012).Environmental variables that are more spatially and temporally variable and unpredictable in streams thanin the hatchery include turbidity, water flow and level and structural complexity provided by, for example,gravel, rocks, plants and trees. Natural fish predators and the prey species diversity of natural streams arelacking in hatcheries where fishes normally are fed pellets (food depicted in grey boxes). Population densityis generally much higher and less variable in the hatchery than in the wild.

At about the same time, on the other side of the globe, in Harrison Hot Springs,British Columbia, Canada, Robertson (1919) was struck by the superior quality andadaptive behaviour of wild sockeye salmon Oncorhynchus nerka (Walbaum 1792)fry relative to fry produced in the hatchery: ‘In strength and capability the differ-ence was as between day and night; the wild natural fry hugged the shore singly orin very small schools, and when pursued made for a hiding place with frenzied erraticdashes. Hatchery fry when liberated swam aimlessly about, and only after repeatedonslaughts of trout and ducks, during which they lost heavily, were they herded intoshallow water’.

S E L E C T I O N I N T E N S I T Y

The differences between wild and hatchery fry observed by Robertson (1919)were partly influenced by selection intensity, i.e. he only observed the best adaptedsurviving fry as the majority of the wild offspring probably died prior to his obser-vations (Jonsson & Fleming, 1993; Elliott, 1994), whereas the hatchery fry hadbeen artificially carried through the intense selection on early vulnerable stages inthe protected hatchery environment, suffering only low mortality (Elliott, 1989).For example, survival from egg to smolt stage is usually 85–95% in the hatcherybut only 1–5% in the wild (Reisenbichler et al., 2004). This difference in mortality



between captive and wild environments was a strong argument for continuation ofstocking practices in the early 20th century (Lydell, 1921), but is today recognizedas an important explanation to why hatchery-reared fishes generally have reducedfitness in the wild (Einum & Fleming, 2001). Even if economic aspects were ignored,it would still be very difficult for a manager to impose more intense nature-likeselection in the hatchery since selective regimes in the wild vary unpredictably dueto fluctuating and frequency-dependent selection (Endler, 1986). Thus, there wouldbe no universal method available for picking out a minority of winner genotypes withthe highest fitness in the wild at a given time. The best option available is to minimizethe time spent in captivity, and release the fishes at an early stage, i.e. as eggs orfry to minimize environmental effects of the hatchery, although there would still bepotential effects due to the lack of mate choice (Neff & Pitcher, 2005). Indeed, studiessuggest that sea-ranched brown trout Salmo trutta L. 1758 can perform as well aswild conspecifics can perform when planted as eyed eggs (Dannewitz et al., 2003). Inregulated catchments, however, early release is generally not efficient as the nursingareas often are deteriorated or completely lacking (Merz et al., 2004). In addition, asfry mortality in the wild is generally very high, unrealistically large numbers of eggor fry often need to be planted to achieve any measurable effects.

P H E N OT Y P I C P L A S T I C I T Y A N D L E A R N I N G

Both Robertson (1919) and Sörensen (1919) were early observers of the effectsof phenotypic plasticity (Pigliucci, 2001), the ability of the phenotype to respond toenvironmental variation. Phenotypic plasticity aids hatchery rearing in the sense that itgenerally helps the offspring of wild fishes adjusting to the evolutionary novel featuresof the hatchery environment. Phenotypic plasticity, however, is limited by reactionnorms (Stearns, 1989), i.e. how the genotype transforms environmental variation tophenotypic variation [Fig. 2(a)] and there is a limit to the range of environments fishescan acclimatize to. Phenotypic development, particularly behavioural development(Wiley et al., 1993; Salvanes & Braithwaite, 2006), is strongly influenced by learningexperiences in the early-life environment (Shumway, 1999; Huntingford, 2004), e.g.encounters with predators (Smith, 1997), interactions with conspecifics (Brown &Laland, 2003) and experience of natural prey (Sundström & Johnsson, 2001; Jacksonet al., 2014) and spatially complex habitats (Braithwaite & Salvanes, 2005). If hatch-ery fishes are not offered any opportunities to learn these life skills prior to releasein the wild, their fitness is likely to be impaired, which also has been found in manystudies (Shumway, 1999; Kellison et al., 2000).

H OW H AT C H E R I E S D I F F E R F RO M T H E W I L D

Compared with most natural environments, artificial rearing environments are homo-geneous and impoverished, something fish biologists have been aware of for a longtime. Schuck (1948) reviewed and listed a number of possible features of the hatcheryenvironment that probably contribute to the low survival of hatchery-reared salmonidsreleased for angling, the list is provided below with its original wording. Althoughhatchery rearing methods have developed in many respects since the 1940s, many ofthe problems addressed today are strikingly similar to those listed by Schuck (1948)below. The following can be added to the list below: (11) absence of sensory stim-ulation (Blaxter, 1970), (12) absence of physical structure (Salvanes et al., 2013) as


1950 J . I . J O H N S S O N E T A L.

Experienced environment

Phen

otyp

e

HN

N

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H

(c)

N

NH

H

(d)

H

NH

N

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H

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Fig. 2. Hypothetical reaction norms showing how environmental variation (x-axis) is translated to phenotypicvariation (y-axis) for a specific genotype (modified from Stearns, 1989). For simplicity, the reaction normis here depicted as a straight line (reaction norms may alternatively be curved, for example, if phenotypicresponses are more canalized at environmental extremes). Distributions represent an environmental variableand its associated phenotypic distribution for natural ( ) and hatchery ( ) environments. (a) The envi-ronmental variation in the hatchery is lower than the natural variation but falls within the same range. Thisrelation is mirrored in the resulting phenotypic distribution where the capacity of the hatchery phenotypeto respond to natural environmental variation is reduced (Piersma & Drent, 2003). (b) The variation in thehatchery environment is increased by enrichment resulting in higher phenotypic trait variation with highercapacity to respond to variation in the natural environment. (c) The environmental variation in the hatcheryfalls outside the range of natural variation to which the organism is evolutionarily adapted which is reflectedin a maladapted phenotype (Ghalambor et al., 2007). (d) The hatchery environment is altered to increasethe similarity with the natural environment resulting in a more adaptive phenotypic response.

well as (13) unnaturally high rearing densities (Brockmark et al., 2010) in conventionalhatcheries and the list would be more or less complete. Examples of recent studies thataddress each of Schuck’s (1948) points have been added to illustrate how valid theystill are: (1) high percentages of fats and carbohydrates in diets (Larsson et al., 2012);(2) overfeeding, which leads to detrimentally high growth rates (Noble et al., 2007);(3) relative lack of exercise (Hoffnagle et al., 2006); (4) artificial conditions where lit-tle foraging for food is necessary (Brockmark et al., 2010); (5) relative freedom frompredators (Johnsson et al., 2001); (6) stable water temperatures (Werner et al., 2006);(7) continued domestication of hatchery breeder (Araki et al., 2007); (8) intentionaland unintentional selection of brood fishes for good hatchery performance, i.e. rapidgrowth and high egg production (Einum & Fleming, 2001); (9) absence of live natural



food (Sundström & Johnsson, 2001); (10) suboptimal transport and release procedures(Strand & Finstad, 2007).

R E AC T I O N N O R M S I N T H E H AT C H E RY A N D I N T H E W I L D

Consider again the concept of the reaction norm to illustrate some general prob-lems of conventional captive and hatchery environments and potential solutions to theseproblems. When hatchery fishes are kept in captivity for several generations, reactionnorms will evolve as a result of inadvertent selection for non-targeted traits that aresimply advantageous in captivity (Waples, 1999) resulting in genotypic and pheno-typic modifications away from the original wild-type, not least in behaviour which isone of the first traits to be affected by domestication (Mayr, 1963; Kohane & Parsons,1988; Sundström et al., 2004). In addition, it has recently been suggested that acquiredbehavioural changes, e.g. induced by captive stress, can be transmitted over generationsby means of epigenetic mechanisms (Jensen, 2013; Evans et al., 2014). Also, even ifwild parents often are used in conservational hatcheries, the lack of mate choice maystill limit the fitness of hatchery-reared offspring (Neff & Pitcher, 2005; Consuegra& Garcia de Leaniz, 2008). Keeping these limitations in mind, the discussion belowwill be restricted to environmental influences on captive-reared offspring of wild par-ents. Reaction norms, describing how environmental variation may be transformed tophenotypic variation for a certain wild-type genotype, are shown in Fig. 2. There aretwo main features of the captive environment that can influence the development offishes reared for release into the wild: environmental variability and environmentalsimilarity.

Environmental variabilityFirstly, the variability of abiotic and biotic factors is generally much lower in the

hatchery than in the wild. Thus, even if the hatchery conditions for the variable in ques-tion (e.g. temperature or current speed) should fall within the range of natural variation[as in Fig. 2(a)], hatchery phenotypes are predicted to be less able to cope with thefull range of variation in the natural environment upon release than wild conspecificssimply because phenotypic capacity will mirror environmental variation during devel-opment (Piersma & Drent, 2003). A potential solution to this problem is to increaseenvironmental variability in the hatchery [Fig. 2(b)], which could be feasible if thefactors in question could be altered in a cost-efficient and manageable fashion. Note,however, that imitating natural environments can be very difficult, and does more harmthan good if carried out in an inappropriate way (Baynes & Howell, 1993; Tuckey& Smith, 2001; Gwak, 2003; Mikheev et al., 2005). Successful alterations requirespecies-specific biological knowledge as well as a detailed understanding of all featuresof the rearing facility.

Environmental similaritySecondly, conventional captive environments may expose the fishes to rearing con-

ditions outside the range of environmental variation to which they are evolutionaryadapted (Schmalhausen, 1949; Blaxter, 1970; Ghalambor et al., 2007). Such condi-tions (e.g. constant overfeeding, unnaturally high densities and sensory deprivation) arelikely to result in development of phenotypes that are maladapted to the wild [Fig. 2(c)].


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The straightforward response to this is to modify rearing conditions to increase sim-ilarity to the natural environment [Fig. 2(d)]. Again, successful modification requirescareful consideration of the biology of the species used and consequences and costs forrearing routines need to be evaluated. For example, reducing rearing density may becomparatively simple to carry out but will increase the production cost per fish, whereasfeeding reduction actually reduces food costs, but needs to be monitored carefully togive intended effects (Jobling et al., 2012).

IMITATING NATURE: DOES IT WORK?

‘Fish aimed for stocking in the wild [… ] should be prepared for a life inthe wild, which requires well-developed learning skills in, for example, for-aging and avoiding predators. These fish should have the species-specificbehavioural repertoire of a wild fish’

Brännäs & Johnsson, 2008

The reasoning above indicates that there is some scope for modifying conventionalrearing environments to better prepare fishes for release into the wild. At the same time,it is clear that the natural environment can never be fully mimicked in a captive envi-ronment, even if technically possible (which it is not simply due to restricted space)the costs would be far too high. Thus, in reality, the challenge is to identify key mod-ifications of the artificial rearing environment that are practically and economicallyfeasible and efficiently promote development towards a more wild-like phenotype. Dosuch key modifications really exist? A variety of methods to improve the post-releaseperformance of captive fishes have been suggested, including various types of envi-ronmental enrichment (Näslund & Johnsson, 2014), life skills training (Suboski &Templeton, 1989; Wiley et al., 1993; Brown & Laland, 2001), pond rearing (Ahlbeck& Holliland, 2012), improved transport and release procedures (Jonsson et al., 1999;Strand & Finstad, 2007), exercise (McDonald et al., 1998; Ward & Hilwig, 2004) andvarious combined approaches (D’Anna et al., 2012; Hyvärinen & Rodewald, 2013).Two main modifications, physical enrichment and density reduction and their influ-ence on behavioural development and subsequent performance in the wild, will beconsidered below. Most, but not all, examples will be from salmonids as this is themost well-investigated fish family in this research area.

P H Y S I C A L E N R I C H M E N T

Environmental enrichment can have many definitions depending on the goal (Young,2003). Here, the discussion is limited to physical enrichment: modifications oradditions of physical structure to the tanks, i.e. increasing structural complexity.The effects of physical enrichment on captive fishes have recently been reviewedby Näslund & Johnsson (2014). Far from attempting another complete review, themain focus will be on the various explanations put forward to explain why physicalenrichment should influence phenotypic and, particularly, behavioural development,and some of the most interesting laboratory and field studies evaluating these ideasare discussed.



Increasing variabilityThe simplest explanation to why physical enrichment should be beneficial in the

captive environment relates to the reaction norms [Fig 2(b)], i.e. the general idea thatphenotypic flexibility mirrors environmental variation (Piersma & Drent, 2003). Thus,if the environment is made more variable by enrichment, the phenotype is expectedto develop a higher capacity to respond to environmental variation, which in turn mayincrease fitness in the more or less unpredictable natural environment encountered afterrelease (Maynard et al., 2004). Physical enrichment may also address the second gen-eral problem with the hatchery environment, i.e. in a general sense making the hatcheryenvironment more similar to nature [Fig. 2(d)]. Although these explanations are intu-itively appealing, they do not offer any specific mechanisms to explain why physicalenrichment should be beneficial for behavioural development.

Saving energyAn important aspect of physical structure is its potential to reduce energy expen-

diture, for example, by providing shelter against current, an ecologically importantfeature for stream-living fishes, which intercept drifting prey from a current-protectedresting position [Allouche, 2002; Fig. 3(a)]. In Atlantic salmon Salmo salar L. 1758,even the mere presence of a shelter (i.e. not necessarily the utilization of it) appearsto have positive effects by reducing basal metabolic rate (Millidine et al., 2006). Forsalmonid alevins (yolk-sac fry), structural support is of critical importance, explaining

(a) Saving energy (b)

(c) (d)

Sheltering behaviour

Neural growth Learning

Fig. 3. Potential effects of introducing physical structure to captive environments. (a) Saving energy by restingbehind or on a structure. (b) Sheltering to avoid or mitigate conspecific aggression and other environmentalstressors. (c) Neural growth as a consequence of direct sensory enrichment induced by physical structureand indirect effects of enhanced opportunity to develop cognitive skills, i.e. (d) learning.


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why this life stage is the most studied when it comes to investigating the effect of struc-ture. Addition of structured incubation substrata is generally beneficial for salmonidalevins and they also prefer substrata over barren floor in choice experiments (Marr,1963; Benhaïm et al., 2009). The most typical effects are related to growth and survival(Taylor, 1984) and are partly mediated by behavioural (i.e. activity) changes. In moststudies on salmonid alevins, structured incubation substrata promote growth primarilyby increasing yolk utilization efficiency. This is mainly due to energy savings medi-ated by reduced swimming activity (Hansen et al., 1990). Incubation substratum alsoincreases survival by mitigating yolk-sac deformation. Due to the high activity levelsof barren-reared alevins, the yolk sac becomes more elongated and thereby more eas-ily constricted. As a result, the fishes are more likely to abrade and rupture the sacsagainst the floor (Emadi, 1972; Hansen & Møller, 1985). Barren-reared alevins alsotend to adopt a vertical head-down position (Emadi, 1972; Murray & Beacham, 1986),which causes relocation of the oil droplet in the yolk sac from the anterior or cen-tral part of the sac to the posterior end, resulting in constriction and deformation ofinternal organs (Emadi, 1972). Not all species show increases in yolk-sac deforma-tions in barren environments, the variation mainly depending on species differencesin alevin activity (Emadi, 1972). Moreover, the frequency of yolk-sac constrictions isdependent on rearing density with more constrictions at higher densities (Murray &Beacham, 1986). The increased activity in barren troughs mainly appears to be causedby the low static stability in the vertical plane. In contrast to alevins resting on substrata,yolk-sac alevins on plain bottoms easily roll over and therefore need to swim to main-tain equilibrium (Marr, 1963; Dill, 1977; Benhaïm et al., 2009). These effects may befurther pronounced by disturbances in the hatchery environment where structure mayhelp buffering alevins against stress-induced activity increases (Hansen et al., 1990).

In general, energy-saving aspects of physical enrichment are facilitated by allowingexpression of species-specific natural behaviours. For example, sand substrata allowbenthic species such as Dover sole Solea solea (L. 1758) to express burying behaviourwhich reduces respiration rate and resting metabolic rate indicating that sandy sub-strata provide less stressful environments (Peyraud & Labat, 1962; Howell & Canario,1987). If environmental enrichment saves energy, generally positive effects on growthon most species and life stages would be expected, everything else being equal. Thegrowth-mediating effects of structure, however, have been found to vary considerablyincluding positive, negative or no effects, depending on species and developmentalstage, which probably reflects the ecology of the species in question (Näslund & Johns-son, 2014). Even if structure often reduces energy expenditure, this effect may becounteracted by structure-induced reductions in the efficiency of food dispersal in thehatchery, as well as limitations of the visual field preventing the fishes from detect-ing food. Also, structure may simply stimulate the innate propensity to hide resultingin reduced food intake (Näslund & Johnsson, 2014). Note, however, that to preparehatchery fishes for life in the wild, it is often more critical to facilitate the developmentof adaptive behaviour than maximizing growth in captivity, and in some cases unre-stricted growth may have negative effects on post-release performance, for example,on migratory behaviour in released smolts (Lans et al., 2011).

Sheltering behaviourAdded shelters are often utilized by captive fishes [Fig. 3(b)], where the effects,

not surprisingly, are most pronounced in species that depend on shelters in their



natural environment (Brown et al., 1970; Slavík et al., 2012). Shelters have beenshown to reduce stress (as indicated by plasma concentrations of cortisol) in SouthAmerican catfish Rhamdia quelen (Quoy & Gaimard 1824) (Barcellos et al., 2009)and S. salar (Näslund et al., 2013). In the latter study, the effect was proposed tobe caused by reduced effect of intermittent stressors and avoidance of conspecificaggression, as the level of dorsal-fin deterioration was lowered compared with barrentanks (Näslund et al., 2013). Similar effects on fin damage have been reported in othersalmonid species such as cutthroat trout Oncorhynchus clarkii (Richardson 1837)and rainbow trout Oncorhynchus mykiss (Walbaum 1792) (Bosakowski & Wagner,1995; Arndt et al., 2001; Berejikian & Tezak, 2005). Reductions in fin deteriorationmay also depend on reduced abrasion with the environment, but in salmonids effectson the dorsal fin are generally assumed to result from aggression. Thus, shelter maygenerally protect from conspecific aggression, and also from intra-specific predationas indicated by several studies on cannibalistic catfish species (Hecht & Appelbaum,1988; Hossain et al., 1998; Coulibaly et al., 2007). As expected, rearing with shelteralso increases the propensity to shelter in novel environments in S. salar (Robertset al., 2011; Näslund et al., 2013), Atlantic cod Gadus morhua L. 1758 (Salvanes &Braithwaite, 2005), black-spot tuskfish Choerodon schoenleinii (Valenciennes 1839)(Kawabata et al., 2010) and white seabream Diplodus sargus (L. 1758) (D’Anna et al.,2012) which may improve post-release survival of fishes released into natural waters.

In territorial and aggressive species, provision of physical structure may not only pro-tect from stress and conspecific aggression; introduction of structural complexity canalso alter the relative fitness of alternative behavioural strategies, for example, betweenaggressive dominants and subordinate individuals. In a mesocosm experiment, Höjesjöet al. (2004) found that addition of rocks and gravel in the habitat increased growthand survival of subordinate S. trutta fry relative to aggressive dominants. Such effectsare yet to be demonstrated under full-scale hatchery conditions but may provide aninteresting opportunity to facilitate coexistence in captivity among a wider range ofbehavioural strategies (i.e. phenotypes), which may increase the overall adaptability tothe environmental variability encountered upon release [Fig. 2(b)].

Neural developmentNeural development is a fundamental basis for developing adaptive behaviour

[Fig. 3(c)]. Experiments on rodents have shown that environmental enrichment stim-ulates neural growth and memory (van Praag et al., 2000). Such effects may be evenmore important in fishes where neurogenesis continues throughout life under theinfluence of environmental experience (Zupanc, 2008). Marchetti & Nevitt (2003)found that several brain structures were smaller in size relative to body size in hatcheryfishes than in wild conspecifics, but they could not separate if these effects weregenetic or environmental. Later studies have shown that physical enrichment increasesthe relative size of the brain, or substructures of the brain, in salmonid fry (Kihslinger& Nevitt, 2006; Näslund et al., 2012). Whether it is the size of the whole brain, or onlythe size of specific substructures of the brain, being affected by enrichment differslargely among studies, making it hard to draw conclusions. It should also be men-tioned that studies on gross size of the brain, or its substructures, do not provide directevidence for increased brain-cell proliferation, as neurogenesis may not reflect itselfas a direct increase in brain size (Lema et al., 2005). Evidence for increased forebraincell proliferation in structurally enriched environments have also been provided (von


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Krogh et al., 2010; Salvanes et al., 2013). Furthermore, altered brain size does notnecessarily translate into behavioural differences, but a few studies suggest that thismay indeed be the case (Burns & Rod, 2008; Kotrschal et al., 2013).

Potential mechanisms for the larger brain size and higher brain cell proliferation inenriched environments could be stimulation of brain growth due to a higher level ofcomplexity, but it may also be effects of lowered social and environmental stress in themore complex environment (Sørensen et al., 2013), or it may be side effects of alteredbody growth patterns.

Kihslinger & Nevitt (2006) hypothesized that environmental enrichment during anearly critical stage (i.e. the alevin stage) could have lasting effects on neural growthand proliferation. This hypothesis was not supported in a follow-up study by Näslundet al. (2012), showing that brain growth in salmonids is plastic. Similar to the study byKihslinger & Nevitt (2006), an early effect of enrichment on brain size was found inS. salar alevins, but the effect gradually disappeared when the developing fry weremoved to conventional rearing tanks. In addition, comparing the brain size of smoltsreleased into the wild with smolts kept in the hatchery revealed that the latter hadrelatively larger brain size, contrary to what is predicted if brain growth is stimulatedby environmental complexity (Näslund et al., 2012). Similar results have been foundwhen comparing brains of hatchery coho salmon Oncorhynchus kisutch (Walbaum1792) reared in semi-natural environments with conspecifics from standard hatcherytanks (Kotrschal et al., 2012). Thus, it appears like releasing hatchery fishes into thewild may not necessarily lead to stimulation of their brain growth, as the results areopposite to what are observed when comparing wild with hatchery fishes (Marchetti& Nevitt, 2003). These counter-intuitive results may potentially be explained byenvironment-specific trade-offs between somatic and neural growth.

Growth rate tends to have an effect on the size of neural structures in relation tothe body size, with slow growing fishes having relatively larger brains (Pankhurst& Montgomery, 1994; Devlin et al., 2012). Part of the explanation for differencesin brain size between wild and hatchery fishes, and between enriched and standardhatchery-reared fishes, could possibly lay in differences in growth rate, body size anddevelopmental stage. Hatchery fishes generally have smaller heads in relation to theirbodies than wild conspecifics (Fleming et al., 1994; Vehanen & Huusko, 2011), whichprobably could be due to a faster somatic growth relative to the head (Currens et al.,1989; Devlin et al., 2012), and this probably contributes to their relatively smallerbrains. Substructures of the brain grow allometrically in relation to body size, par-ticularly during the alevin and fry stage (Näslund et al., 2012), and slight differencesin size or developmental stage among the compared groups may lead to significant dif-ferences in brain structures. There is also allometric change in the brain size duringsmolt transformation in salmonids (Ebbesson & Braithwaite, 2012). Further investiga-tions are clearly needed to elucidate the growth trade-offs between body and brain andhead in relation to genetic background and rearing environment, and the effects of suchtrade-offs on behaviour.

LearningSeveral recent studies support the hypothesis that environmental enrichment can

improve cognitive ability, including learning and general adaptability, to novel con-ditions [Fig. 3(d)]. For instance, physical enrichment has positive effects on bothneurogenesis and learning in S. salar trained to escape a maze, importantly suggesting



that neurogenesis could be linked to biologically relevant life skills (Salvanes et al.,2013). Wild-type strains of zebrafish Danio rerio (Hamilton 1822) also appear to learnfaster in enriched environments than in simple environments (Spence et al., 2011) andseveral studies on G. morhua show that in-tank structures increase behavioural flexibil-ity as well as social learning (Braithwaite & Salvanes, 2005; Salvanes & Braithwaite,2005; Strand et al., 2010). All types of increases in environmental variation are notnecessarily beneficial. For example, Lee & Berejikian (2008) found that enrichmentwith stones and plastic plants promoted explorative behaviour in O. mykiss whentank structures were stable over time. This effect disappeared when structures variedover time, probably due to stress effects caused by frequent disturbance. Moreover,environmental enrichment improved foraging efficiency on novel prey in S. salar, butonly if the fish also had previous experience of live food (Sundström & Johnsson,2001; Brown et al., 2003).

D E N S I T Y R E D U C T I O N

Primarily for economic reasons, captive rearing densities are almost invariably higherthan natural densities. Thus, an obvious effect of most density reductions will be tomake the environment more nature-like which may be generally beneficial to promotedevelopment towards a nature-like phenotype [Brännäs & Johnsson, 2008; Fig. 2(d)].Although density effects have been well studied in fish farming, research has tradition-ally been focused on crowding stress, including welfare-associated stress measuresas fin damage and cortisol measurements (Ellis et al., 2002). Altering rearing den-sities may also have profound influence on behavioural development (Brockmark &Johnsson, 2010; Brockmark et al., 2010). Some recent progress in behavioural and cog-nitive research is highlighted to suggest mechanisms through which density may affectthe behaviour of captive fishes. The few empirical studies in which effects of densityon behavioural development have been specifically investigated are also discussed. Insome respects, density can actually be thought of as a form of structure. In fact, inpelagic environments, schools may provide associated individuals with several advan-tages resembling those of physical structures, including hydrodynamic savings as wellas shelter from predation (Krause & Ruxton, 2002). Density effects on neural develop-ment are still poorly investigated, but may share similarities with the effects inducedby physical enrichment. In addition, density may influence cognition and behaviourin captive fishes through quite different mechanisms than structure, for example, bydensity-mediated effects on social interactions (Sørensen et al., 2013).

Crowding stressIn intensive fish farming, the effects of stocking density have been extensively

studied for a number of traits, but with variable results, suggesting that many factorsinteract with density to affect performance in a hatchery (Ellis et al., 2002; Brännäs &Johnsson, 2008). In several salmonid species, adverse effects of high stocking densityas reductions in survival, food conversion efficiency and growth, as well as increasesin fin damage have been reported (Brännäs et al., 2001; Ellis et al., 2002; Brockmarket al., 2007). These effects have tentatively been ascribed to stress responses causedby crowding [Baker & Ayles, 1990; Fig 4(a)]. Some of the negative effects on growthmay be due to reduction of feeding efficiency rather than chronic stress. For example,increased density can induce scramble competition where individuals simply are


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getting in the way of each other, increasing losses of food from the hatchery tank(Ruxton, 1993). Similarly, high density may induce shadow interference, whereindividuals experience reduced food intake from being shadowed by competitors(Elliott, 2002; Krause & Ruxton, 2002). These effects may be more or less severedepending on how the species in question feed naturally. For example, Arctic charrSalvelinus alpinus (L. 1758), which is a naturally schooling species, adapt well tocrowding (Brown et al., 1992; Jørgensen & Jobling, 1993). Many flatfish species useprimarily two-dimensional rather than three-dimensional space and rest on the bottomrather than school. Thus, stocking density of flatfishes is limited by tank bottomarea rather than volume and negative effects on growth performance and survivalhave been found in S. solea, (Schram et al., 2006) and Atlantic halibut Hippoglossushippoglossus (L. 1758) (Kristiansen et al., 2004). Tank bottom area is also importantin captive rearing of salmonids, as the natural juvenile behaviour of many species isto reside close to the bottom (Yamagishi, 1962). In gilthead seabream Sparus aurataL. 1758, high stocking densities increased chronic stress, as indicated by elevation ofplasma cortisol and associated adverse effects on biochemical composition, immunestatus and haematology (Montero et al., 1999). Growth rate, however, was not affectedwhich illustrates the potential problem of relying solely on growth performance asa general welfare indicator in aquaculture. For fishes to be released into the wild,minimizing stress in captivity is not sufficient and may not even be the primary goalas individuals need to be prepared for a post-release environment that is often harshand unpredictable (Brännäs & Johnsson, 2008).

Resource defenceTerritorial behaviour is widespread in fishes including species used for stocking, such

as salmonids, where territorial behaviour and resource defence have been well studied[Grant, 1997; Fig. 4(b)]. Everything else being equal, territorial defence is expected todecrease with increasing rearing density as the economic defendability of a territoryis inversely related to competitor pressure (Grant, 1997). Consequently, some stud-ies on farmed species such as African sharptooth catfish Clarias gariepinus (Burchell1822) have found that high densities reduce agonistic behaviour (Kaiser et al., 1995;Hecht & Uys, 1997). Density effects on competition, however, can be more complexthan just altering aggression levels. In another study on S. alpinus and O. mykiss, usinga self-feeding setup, dominance rank remained unchanged with increasing competi-tor density, but the relative payoffs of high-ranking individuals decreased (Alanärä &Brännäs, 1996). There is evidence that hatchery-reared fishes, even when sharing thesame genetic background, are less effective in aggressive contests than wild fishes.For example, hatchery-reared S. trutta invest more time and energy in territorial con-flicts than wild conspecifics without increasing their probability of winning (Deverillet al., 1999; Sundström et al., 2003). It is not known whether these effects are due toenvironmental effects on phenotypic development, or differences in selection intensitybetween the hatchery and the natural environment, as discussed previously.

There is, so far, only one study specifically investigating the link between rearingdensity, individual competitive ability and post-release performance in the wild(Brockmark & Johnsson, 2010). The authors found that S. trutta parr reared at naturaldensity (based on density estimates by Elliott, 1994) had significantly higher domi-nance rank when competing with fish reared at conventional, and half of conventionalrearing densities. Interestingly, the dominance in low-density trout was due to superior



(a) Crowding stress (b) Resource defence

?

(c) Individual recognition (d) Individual decision

Fig. 4. Potential effects of rearing density in captive environments. (a) High density may increase crowding stressdue to, for example, increased conspecific aggression, abrasion and loss of individual sensory control. (b)The potential for (practising) resource defence is dependent on rearing density. (c) The cognitive abilityto learn and remember individual identities is limited by rearing density, i.e. the number of individualsencountered. (d) Rearing density may influence the benefits of performing and learning individual behaviourdue to its effects on visual restriction, shadow competition and physical obstruction.

ability to monopolize food rather than overt aggression. Subsequent release into astream section with natural predation revealed that the competitive superiority oflow-density S. trutta was translated to increased growth and survival (see Fig. 5;post-release effects). These results suggest that reduced rearing density facilitates thedevelopment of adaptive behaviour, acquiring life skills that increase post-release fit-ness. The underlying mechanisms remain speculative. Are the effects due to increasedpotential for learned resource defence and contest behaviour at lower densities, or arethere other mechanisms at play as well?

Individual recognitionEnvironmental effects on social behaviour, as demonstrated above by Brockmark &

Johnsson (2010), may also be mediated by limited attention abilities that constrain theamount of environmental information that can be processed by animals (Desimone &Duncan, 1995; Dukas, 2002). Social behaviour is probably facilitated by the devel-opment of familiarity with other individuals over time, which in turn is limited by thenumber of individual identities that can be learned and memorized, as well as the oppor-tunity for learning, i.e. how frequently a specific individual is encountered (Griffiths& Ward, 2011). Thus, in a high-density environment, there is little scope to developsocial relations with specific individuals, which may impair the development of social


1960 J . I . J O H N S S O N E T A L.

0 500 1000 1500 2000 25000

20

40

60

Density (individuals m-2)

Pos

t-re

leas

e su

rviv

al (

%)

Fig. 5. The relation between rearing density and post-release survival in a natural stream section (estimated byrecapture rate) in Salmo trutta parr. Data are based on Brockmark & Johnsson (2010) ( ) and Brockmarket al. (2010) ( , rearing with added physical structure; , no structure). Fish in both studies were rearedin the hatchery treatments from the egg stage and released into the stream c. 4⋅5 months after first feeding.The curve was fitted by: y=−0⋅0104x+ 44⋅505 (r2 = 0⋅78, P< 0⋅01).

behaviour [Fig. 4(c)]. Hypothetically, physical enrichment could have similar effectsby dividing the rearing environment to smaller units consistently utilized by a limitedsub-sample of individuals. Previous studies have shown that familiarity can increasefood intake, reduce aggression and increase vigilance towards predation threat in S.trutta groups, suggesting a link between individual recognition, social competence andfitness (Höjesjö et al., 1998; Griffiths et al., 2004).

Individual decisionAn alternative, not mutually exclusive, explanation suggested by Brockmark et al.

(2010) is that high-density conditions in captivity may alter the trade-off betweenusing private and public information [Laland, 2004; Brown & Laland, 2011; Fig. 4(d)].Indeed, human studies show that individuals react to long-time crowding by graduallyreducing individual control (Bell et al., 2001). Moreover, theoretical analyses (Rogers,1988; Giraldeau et al., 2002) as well as empirical studies on fishes (van Bergen et al.,2004) suggest that a combination of private and public information use is critical foradaptive decision-making. Thus, high-density conditions that constantly favour theuse of public information over ontogeny might lead to conformity where individu-als gradually lose their inherent capacity for independent decision-making. Environ-mental effects on cognitive and behavioural development, as discussed above, mayhelp explain the strong density effects on adaptive behaviour (i.e. life skills) found byBrockmark et al. (2010) where S. trutta parr reared at natural or a fourth of conven-tional rearing density showed increased ability to feed on novel prey, improved spatialorientation in a food maze and more efficient anti-predator behaviour, i.e. sheltering inresponse to a simulated predator attack. Again, the improved behavioural performancewas mirrored by increased post-release survival in a natural stream section comparedwith fish reared at conventional densities (Fig. 5).



P O S T- R E L E A S E E F F E C T S

The success of releasing animals into an unfamiliar environment is dependent on theirphenotypic plasticity and the range of environments to which acclimation is possibleis limited by genetic and developmental constraints (Pigliucci, 2001; Fig. 2). Releasedfishes often have poor survival in the wild (Olla et al., 1998; Brown & Laland, 2001;Melnychuk et al., 2014) and frequently show impaired post-release performance inother traits, e.g. feeding (Gil et al., 2014) and migration accuracy (Kennedy et al.,2013). Performance in the wild can be improved by allowing acclimation to the naturalenvironment before release (so-called soft release) or by improved (i.e. less stress-ful) transport procedures (Jonsson et al., 1999; Strand & Finstad, 2007). Much of thepost-release mortality occurs shortly after release (McCrimmon, 1954; Thorstad et al.,2011) and surviving fishes gradually adapt better to the wild (Stringwell et al., 2014),suggesting that adaptive traits during this initial period in the wild should be targetedwhen aiming to improve rearing methods for stocked fishes.

Enrichment effectsSeveral studies show that rearing with environmental enrichment increases the

competitive ability of O. mykiss in semi-natural environments (Berejikian et al., 2000,2001; Tatara et al., 2008). In D. sargus, shelters and predator experience increasedestimated sea survival where shelter conditioned fish also dispersed less from therelease point (D’Anna et al., 2012). Enrichment has been found to increase foragingefficiency in juvenile S. salar (Rodewald et al., 2011) and survival of migrating S.salar smolts (Hyvärinen & Rodewald, 2013). Moreover, in a recent study by Robertset al. (2014), enriched juvenile S. salar had higher recapture rates and occupied moreprofitable habitats than conventionally reared fish when they were stocked as age 0+year fry, but not when they were stocked as age 1+ year parr. In these studies on S.salar, several types of enrichment were applied simultaneously, including structuresand water current variability, so their relative importance could not be evaluated. Itshould be pointed out that a number of published studies have failed to demonstrateany significant enrichment effects on post-release performance (Berejikian et al.,1999; Brockmark et al., 2007; Fast et al., 2008; Tatara et al., 2008, 2009; Brockmark& Johnsson, 2010) or show mixed results (Vidergar et al., 2003). Thus, enrichmentdoes not always have ecologically relevant effects and may also be counteractedby other modifications in the rearing environment. For instance, starvation beforerelease may increase activity and risk-taking irrespective of prior rearing environment(Moberg et al., 2011). Other studies also indicate that high rearing densities mayimpair and even reverse the positive effects of physical enrichment (Hoelzer, 1987;Näslund & Johnsson, 2014; unpubl. data).

Density effectsAs discussed previously, reduced rearing density appears to facilitate the develop-

ment of adaptive behaviour in S. trutta parr, resulting in increased post-release sur-vival and growth in their natural stream environment (Brockmark & Johnsson, 2010;Brockmark et al., 2010). Interestingly, combining the effects of the densities used inthese two studies (which were conducted in the same model system and therefore com-parable) suggests that post-release survival is inversely correlated with rearing density


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over the range of densities used (Fig. 5). The question remains whether these benefi-cial effects are specific for territorial parr and thereby limited to the freshwater stage ofanadromous salmonids, or are more general, that is, also beneficial for smolt migrationand post-release survival in the sea. Preliminary data support a general effect wherereduced rearing density has been found to increase seaward migration in 1 year-old S.salar smolts in three separate studies (J. I. Johnsson, unpubl. data). The positive effectsof reduced rearing density on post-release performance are further supported by Barneset al. (2013). In their study, post-stocking harvest and spawning returns of landlockedfall Chinook salmon Oncorhynchus tshawytscha (Walbaum 1792) were consistentlyimproved by reducing rearing density. Other studies on Pacific salmonids have foundvariable effects of rearing density where differences may be attributed to species dif-ferences, variation in rearing facilities (e.g. ponds v. raceways) and other sources ofenvironmental variation (Ewing & Ewing, 1995; Tipping et al., 2004).

CONCLUSIONS

To come back to the first general question asked at the beginning of this paper: isit feasible to try to mimic key aspects of natural conditions in a full-scale hatcheryto produce fishes better adapted to the wild? The short answer to this question is:yes. Accumulating evidence summarized in this and other papers suggests that rela-tively simple environmental modifications of captive environments can significantlyalter phenotypic development of fishes, including effects on neural growth, physiol-ogy and behaviour. Here, the focus has been on physical structure and rearing density,two critical features of the captive environment that can mediate phenotypic effects.If environmental modifications are adequately adapted to species-specific and localconditions, they can help produce a more wild-like fish with improved post-releaseperformance. This also partially answers the second question: could studies in artificialenvironments such as aquaria or hatchery tanks predict how fishes will perform in thewild? The short answer is again yes. Several recent studies have shown a link betweenadaptive behavioural changes in captivity and post-release performance (Brockmarket al., 2010). That said, there is still a lack of studies combining laboratory and fieldapproaches to investigate how phenotypic changes in the captive environment influ-ence post-release fitness, an important challenge for future research. It should also bestressed that the success of modifications of captive environments has been found to behighly variable. For example, many studies evaluating physical enrichment have foundno or even negative effects (Näslund & Johnsson, 2014).

To be accepted in full-scale commercial operations, biologically sound modifica-tions of captive environments also need to be economically feasible (Horreo et al.,2012). For example, reducing rearing densities will increase the production cost perfish and therefore needs to increase post-release survival and returns of stocked fishesto meet increased production costs. Similarly, introduction of physical structure in cap-tive environments may increase cleaning costs as well as the risk of infections. In manycountries, however, there is a growing public concern, as well as increasingly strict leg-islation concerning animal welfare where the ultimate goal is to minimize stress andallow natural behaviour to be expressed, the latter goal being the more important onefor stocked fishes.



In summary, it can be concluded that both physical enrichment and reduced den-sity have potential to increase the fitness of hatchery fishes released into naturalenvironments, but the success of these manipulations is strongly dependent onadequately adapting methods to species and life stage-specific conditions. Furtherdevelopment of rearing methods for fishes to be released in the wild should be basedon research applying state-of-the art biological knowledge in a multidisciplinaryframework including economical and societal aspects.

This study was funded by the strategic project SMOLTPRO, financed by the Swedish ResearchCouncil Formas. We thank C. Garcia de Leaniz and an anonymous reviewer for helpful com-ments on the manuscript.

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Electronic Reference

Vidergar, D., Petering, T. & Kline, P. (2003). Chinook Salmon Seminatural Rearing Experiment:Sawtooth and Clearwater Fish Hatcheries, Idaho. Available at http://www.fws.gov/lsnakecomplan/Reports/IDFG/Eval/03-35%20Vidergar%20Chinook%20Seminatural%20Rearing%20Experiment-Nature.pdf/


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