Journal of Fish Biology (2014) 85, 1946–1971
doi:10.1111/jfb.12547, available online at wileyonlinelibrary.com
REVIEW PAPER
Environmental effects on behavioural development
consequences 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 conspecifics, 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 that
optimize post-release performance, as well as to recognize the limitations of what can be achieved
by modifying hatchery rearing methods. Fishes are generally very plastic in their development and
through gene–environment interactions, epigenetic and maternal effects their phenotypes will develop
differently depending on their rearing environment. This suggests that there is scope for modifying conventional rearing environments to better prepare fishes for release into the wild. The complexity of the
natural environment is impossible to mimic in full-scale rearing facilities. So, in reality, the challenge is
to identify key modifications of the artificial rearing environment that are practically and economically
feasible and that efficiently promote development towards a more wild-like phenotype. Do such key
modifications really exist? Here, attempts to use physical enrichment and density reduction to improve
the performance of hatchery fishes are discussed and evaluated. These manipulations show potential
to increase the fitness of hatchery fishes released into natural environments, but the success is strongly
dependent 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 them
and in acclimating in new waters species which are valuable for food or
sport, 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 O T C O V E R
This paper summarizes and discusses results from recent research highlighting the
possibilities as well as the challenges associated with improving the post-release
†Author to whom correspondence should be addressed. Tel.: +46 31 7863665; email: jorgen.johnsson@
bioenv.gu.se
1946
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performance of captive-reared fishes by environmental modification of the captive
environment. Here, welfare (Browman & Skiftesvik, 2007) will not be discussed in
depth. It is enough to stress that fishes show an incredible diversity of adaptations and
where new studies are accumulating evidence of a level of cognitive ability, learning
capacity and environmental sensitivity that was unheard of not many years ago (Brown
et al., 2011). The primary focus is on environmental effects and gene–environment
interactions on hatchery-reared offspring of wild parents. Multi-generational genetic
effects of domestication and artificial selection are very important aspects to understand long-term consequences of stocking and potential effects on wild populations,
but will not be the main focus here. These aspects have been thoroughly addressed
in 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 fish
conservation efforts, and hatchery releases should only be considered in cases where
there 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 and
hatchery fishes could ever be ecologically exchangeable (Bisson et al., 2000; Brannon
et al., 2004), hatchery rearing methods for conservation and supplementation are,
despite a long history, still in their infancy and could potentially be developed to produce 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 temporal
variation 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 natural
conditions in a full-scale hatchery to produce fishes better adapted to the wild? Could
behavioural 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 R O 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 Ludwig
Jacobi in Germany in the mid-18th century, an achievement for which he was rewarded
life pension by King George III of the U. K. Since then, artificially propagated fishes
have been stocked in large numbers in streams, rivers, ponds, lakes and the sea at various stages of development. Originally, these activities were mainly intended to boost
the yield of fishes in stocked waters. Early on, however, fishery managers were aware
of behavioural changes induced by artificial rearing environments. For example, at a
fishery management meeting held on 17 March 1919 in Stockholm the Swedish fishery
instructor Sörensen (1919) stated (free translation from Swedish): ‘These fish [Atlantic
salmon] have become so tame that they are unsuitable to persist in the struggle for survival as it is manifested in nature, including the water [ … ] their innate natural caution
is completely vanished. If you hold a net just below the water surface and throw some
food over it, the fish gather in a school around the food.[ … ] this as an example of how
the shyness of the fish, by which it avoids many dangers, disappears during regular
feeding’.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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(a)
Water level
Turbid
Clear
(b)
Water level
Fig. 1. Some key environmental differences between a (a) natural stream and (b) conventional hatchery environment 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 than
in 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 are
lacking in hatcheries where fishes normally are fed pellets (food depicted in grey boxes). Population density
is 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 and
adaptive behaviour of wild sockeye salmon Oncorhynchus nerka (Walbaum 1792)
fry relative to fry produced in the hatchery: ‘In strength and capability the difference was as between day and night; the wild natural fry hugged the shore singly or
in very small schools, and when pursued made for a hiding place with frenzied erratic
dashes. Hatchery fry when liberated swam aimlessly about, and only after repeated
onslaughts of trout and ducks, during which they lost heavily, were they herded into
shallow water’.
SELECTION INTENSITY
The differences between wild and hatchery fry observed by Robertson (1919)
were partly influenced by selection intensity, i.e. he only observed the best adapted
surviving fry as the majority of the wild offspring probably died prior to his observations (Jonsson & Fleming, 1993; Elliott, 1994), whereas the hatchery fry had
been artificially carried through the intense selection on early vulnerable stages in
the protected hatchery environment, suffering only low mortality (Elliott, 1989).
For example, survival from egg to smolt stage is usually 85–95% in the hatchery
but only 1–5% in the wild (Reisenbichler et al., 2004). This difference in mortality
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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between captive and wild environments was a strong argument for continuation of
stocking practices in the early 20th century (Lydell, 1921), but is today recognized
as an important explanation to why hatchery-reared fishes generally have reduced
fitness 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-like
selection in the hatchery since selective regimes in the wild vary unpredictably due
to fluctuating and frequency-dependent selection (Endler, 1986). Thus, there would
be no universal method available for picking out a minority of winner genotypes with
the highest fitness in the wild at a given time. The best option available is to minimize
the time spent in captivity, and release the fishes at an early stage, i.e. as eggs or
fry to minimize environmental effects of the hatchery, although there would still be
potential effects due to the lack of mate choice (Neff & Pitcher, 2005). Indeed, studies
suggest that sea-ranched brown trout Salmo trutta L. 1758 can perform as well as
wild conspecifics can perform when planted as eyed eggs (Dannewitz et al., 2003). In
regulated catchments, however, early release is generally not efficient as the nursing
areas often are deteriorated or completely lacking (Merz et al., 2004). In addition, as
fry mortality in the wild is generally very high, unrealistically large numbers of egg
or 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 effects
of phenotypic plasticity (Pigliucci, 2001), the ability of the phenotype to respond to
environmental variation. Phenotypic plasticity aids hatchery rearing in the sense that it
generally helps the offspring of wild fishes adjusting to the evolutionary novel features
of the hatchery environment. Phenotypic plasticity, however, is limited by reaction
norms (Stearns, 1989), i.e. how the genotype transforms environmental variation to
phenotypic variation [Fig. 2(a)] and there is a limit to the range of environments fishes
can acclimatize to. Phenotypic development, particularly behavioural development
(Wiley et al., 1993; Salvanes & Braithwaite, 2006), is strongly influenced by learning
experiences 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; Jackson
et al., 2014) and spatially complex habitats (Braithwaite & Salvanes, 2005). If hatchery fishes are not offered any opportunities to learn these life skills prior to release
in the wild, their fitness is likely to be impaired, which also has been found in many
studies (Shumway, 1999; Kellison et al., 2000).
H O W H AT C H E R I E S D I F F E R F R O M T H E W I L D
Compared with most natural environments, artificial rearing environments are homogeneous and impoverished, something fish biologists have been aware of for a long
time. Schuck (1948) reviewed and listed a number of possible features of the hatchery
environment that probably contribute to the low survival of hatchery-reared salmonids
released for angling, the list is provided below with its original wording. Although
hatchery rearing methods have developed in many respects since the 1940s, many of
the 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 stimulation (Blaxter, 1970), (12) absence of physical structure (Salvanes et al., 2013) as
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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(b)
H N
H N
(a)
Phenotype
N H
N
(c)
H
H
N
H N
(d)
N
H
N
H
Experienced environment
Fig. 2. Hypothetical reaction norms showing how environmental variation (x-axis) is translated to phenotypic
variation (y-axis) for a specific genotype (modified from Stearns, 1989). For simplicity, the reaction norm
is here depicted as a straight line (reaction norms may alternatively be curved, for example, if phenotypic
responses are more canalized at environmental extremes). Distributions represent an environmental variable
and its associated phenotypic distribution for natural ( ) and hatchery ( ) environments. (a) The environmental variation in the hatchery is lower than the natural variation but falls within the same range. This
relation is mirrored in the resulting phenotypic distribution where the capacity of the hatchery phenotype
to respond to natural environmental variation is reduced (Piersma & Drent, 2003). (b) The variation in the
hatchery environment is increased by enrichment resulting in higher phenotypic trait variation with higher
capacity to respond to variation in the natural environment. (c) The environmental variation in the hatchery
falls outside the range of natural variation to which the organism is evolutionarily adapted which is reflected
in a maladapted phenotype (Ghalambor et al., 2007). (d) The hatchery environment is altered to increase
the similarity with the natural environment resulting in a more adaptive phenotypic response.
well as (13) unnaturally high rearing densities (Brockmark et al., 2010) in conventional
hatcheries and the list would be more or less complete. Examples of recent studies that
address each of Schuck’s (1948) points have been added to illustrate how valid they
still 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 little foraging for food is necessary (Brockmark et al., 2010); (5) relative freedom from
predators (Johnsson et al., 2001); (6) stable water temperatures (Werner et al., 2006);
(7) continued domestication of hatchery breeder (Araki et al., 2007); (8) intentional
and unintentional selection of brood fishes for good hatchery performance, i.e. rapid
growth and high egg production (Einum & Fleming, 2001); (9) absence of live natural
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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food (Sundström & Johnsson, 2001); (10) suboptimal transport and release procedures
(Strand & Finstad, 2007).
R E A C 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 problems of conventional captive and hatchery environments and potential solutions to these
problems. When hatchery fishes are kept in captivity for several generations, reaction
norms will evolve as a result of inadvertent selection for non-targeted traits that are
simply advantageous in captivity (Waples, 1999) resulting in genotypic and phenotypic modifications away from the original wild-type, not least in behaviour which is
one 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 acquired
behavioural changes, e.g. induced by captive stress, can be transmitted over generations
by means of epigenetic mechanisms (Jensen, 2013; Evans et al., 2014). Also, even if
wild parents often are used in conservational hatcheries, the lack of mate choice may
still limit the fitness of hatchery-reared offspring (Neff & Pitcher, 2005; Consuegra
& Garcia de Leaniz, 2008). Keeping these limitations in mind, the discussion below
will be restricted to environmental influences on captive-reared offspring of wild parents. Reaction norms, describing how environmental variation may be transformed to
phenotypic variation for a certain wild-type genotype, are shown in Fig. 2. There are
two main features of the captive environment that can influence the development of
fishes reared for release into the wild: environmental variability and environmental
similarity.
Environmental variability
Firstly, 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 question (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 the
full range of variation in the natural environment upon release than wild conspecifics
simply because phenotypic capacity will mirror environmental variation during development (Piersma & Drent, 2003). A potential solution to this problem is to increase
environmental variability in the hatchery [Fig. 2(b)], which could be feasible if the
factors 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 harm
than good if carried out in an inappropriate way (Baynes & Howell, 1993; Tuckey
& Smith, 2001; Gwak, 2003; Mikheev et al., 2005). Successful alterations require
species-specific biological knowledge as well as a detailed understanding of all features
of the rearing facility.
Environmental similarity
Secondly, conventional captive environments may expose the fishes to rearing conditions outside the range of environmental variation to which they are evolutionary
adapted (Schmalhausen, 1949; Blaxter, 1970; Ghalambor et al., 2007). Such conditions (e.g. constant overfeeding, unnaturally high densities and sensory deprivation) are
likely 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 similarity to the natural environment [Fig. 2(d)]. Again, successful modification requires
careful consideration of the biology of the species used and consequences and costs for
rearing routines need to be evaluated. For example, reducing rearing density may be
comparatively simple to carry out but will increase the production cost per fish, whereas
feeding reduction actually reduces food costs, but needs to be monitored carefully to
give intended effects (Jobling et al., 2012).
IMITATING NATURE: DOES IT WORK?
‘Fish aimed for stocking in the wild [ … ] should be prepared for a life in
the wild, which requires well-developed learning skills in, for example, foraging and avoiding predators. These fish should have the species-specific
behavioural repertoire of a wild fish’
Brännäs & Johnsson, 2008
The reasoning above indicates that there is some scope for modifying conventional
rearing 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 environment, 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 modifications of the artificial rearing environment that are practically and economically
feasible and efficiently promote development towards a more wild-like phenotype. Do
such key modifications really exist? A variety of methods to improve the post-release
performance of captive fishes have been suggested, including various types of environmental 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) and
various combined approaches (D’Anna et al., 2012; Hyvärinen & Rodewald, 2013).
Two main modifications, physical enrichment and density reduction and their influence on behavioural development and subsequent performance in the wild, will be
considered below. Most, but not all, examples will be from salmonids as this is the
most well-investigated fish family in this research area.
PHYSICAL ENRICHMENT
Environmental enrichment can have many definitions depending on the goal (Young,
2003). Here, the discussion is limited to physical enrichment: modifications or
additions of physical structure to the tanks, i.e. increasing structural complexity.
The effects of physical enrichment on captive fishes have recently been reviewed
by Näslund & Johnsson (2014). Far from attempting another complete review, the
main focus will be on the various explanations put forward to explain why physical
enrichment should influence phenotypic and, particularly, behavioural development,
and some of the most interesting laboratory and field studies evaluating these ideas
are discussed.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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Increasing variability
The 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 that
phenotypic flexibility mirrors environmental variation (Piersma & Drent, 2003). Thus,
if the environment is made more variable by enrichment, the phenotype is expected
to develop a higher capacity to respond to environmental variation, which in turn may
increase fitness in the more or less unpredictable natural environment encountered after
release (Maynard et al., 2004). Physical enrichment may also address the second general problem with the hatchery environment, i.e. in a general sense making the hatchery
environment more similar to nature [Fig. 2(d)]. Although these explanations are intuitively appealing, they do not offer any specific mechanisms to explain why physical
enrichment should be beneficial for behavioural development.
Saving energy
An important aspect of physical structure is its potential to reduce energy expenditure, for example, by providing shelter against current, an ecologically important
feature for stream-living fishes, which intercept drifting prey from a current-protected
resting 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) appears
to have positive effects by reducing basal metabolic rate (Millidine et al., 2006). For
salmonid alevins (yolk-sac fry), structural support is of critical importance, explaining
(a)
Saving energy
(b)
Sheltering behaviour
(c)
Neural growth
(d)
Learning
Fig. 3. Potential effects of introducing physical structure to captive environments. (a) Saving energy by resting
behind or on a structure. (b) Sheltering to avoid or mitigate conspecific aggression and other environmental
stressors. (c) Neural growth as a consequence of direct sensory enrichment induced by physical structure
and 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 structure. Addition of structured incubation substrata is generally beneficial for salmonid
alevins 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 most
studies on salmonid alevins, structured incubation substrata promote growth primarily
by increasing yolk utilization efficiency. This is mainly due to energy savings mediated by reduced swimming activity (Hansen et al., 1990). Incubation substratum also
increases survival by mitigating yolk-sac deformation. Due to the high activity levels
of barren-reared alevins, the yolk sac becomes more elongated and thereby more easily constricted. As a result, the fishes are more likely to abrade and rupture the sacs
against the floor (Emadi, 1972; Hansen & Møller, 1985). Barren-reared alevins also
tend 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 central part of the sac to the posterior end, resulting in constriction and deformation of
internal organs (Emadi, 1972). Not all species show increases in yolk-sac deformations in barren environments, the variation mainly depending on species differences
in alevin activity (Emadi, 1972). Moreover, the frequency of yolk-sac constrictions is
dependent on rearing density with more constrictions at higher densities (Murray &
Beacham, 1986). The increased activity in barren troughs mainly appears to be caused
by 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 maintain equilibrium (Marr, 1963; Dill, 1977; Benhaïm et al., 2009). These effects may be
further pronounced by disturbances in the hatchery environment where structure may
help buffering alevins against stress-induced activity increases (Hansen et al., 1990).
In general, energy-saving aspects of physical enrichment are facilitated by allowing
expression of species-specific natural behaviours. For example, sand substrata allow
benthic species such as Dover sole Solea solea (L. 1758) to express burying behaviour
which reduces respiration rate and resting metabolic rate indicating that sandy substrata provide less stressful environments (Peyraud & Labat, 1962; Howell & Canario,
1987). If environmental enrichment saves energy, generally positive effects on growth
on most species and life stages would be expected, everything else being equal. The
growth-mediating effects of structure, however, have been found to vary considerably
including positive, negative or no effects, depending on species and developmental
stage, which probably reflects the ecology of the species in question (Näslund & Johnsson, 2014). Even if structure often reduces energy expenditure, this effect may be
counteracted by structure-induced reductions in the efficiency of food dispersal in the
hatchery, as well as limitations of the visual field preventing the fishes from detecting food. Also, structure may simply stimulate the innate propensity to hide resulting
in reduced food intake (Näslund & Johnsson, 2014). Note, however, that to prepare
hatchery fishes for life in the wild, it is often more critical to facilitate the development
of adaptive behaviour than maximizing growth in captivity, and in some cases unrestricted growth may have negative effects on post-release performance, for example,
on migratory behaviour in released smolts (Lans et al., 2011).
Sheltering behaviour
Added 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
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natural environment (Brown et al., 1970; Slavík et al., 2012). Shelters have been
shown to reduce stress (as indicated by plasma concentrations of cortisol) in South
American 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 to
be caused by reduced effect of intermittent stressors and avoidance of conspecific
aggression, as the level of dorsal-fin deterioration was lowered compared with barren
tanks (Näslund et al., 2013). Similar effects on fin damage have been reported in other
salmonid 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 deterioration
may also depend on reduced abrasion with the environment, but in salmonids effects
on the dorsal fin are generally assumed to result from aggression. Thus, shelter may
generally protect from conspecific aggression, and also from intra-specific predation
as indicated by several studies on cannibalistic catfish species (Hecht & Appelbaum,
1988; Hossain et al., 1998; Coulibaly et al., 2007). As expected, rearing with shelter
also increases the propensity to shelter in novel environments in S. salar (Roberts
et 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 protect from stress and conspecific aggression; introduction of structural complexity can
also alter the relative fitness of alternative behavioural strategies, for example, between
aggressive dominants and subordinate individuals. In a mesocosm experiment, Höjesjö
et al. (2004) found that addition of rocks and gravel in the habitat increased growth
and survival of subordinate S. trutta fry relative to aggressive dominants. Such effects
are yet to be demonstrated under full-scale hatchery conditions but may provide an
interesting opportunity to facilitate coexistence in captivity among a wider range of
behavioural strategies (i.e. phenotypes), which may increase the overall adaptability to
the environmental variability encountered upon release [Fig. 2(b)].
Neural development
Neural development is a fundamental basis for developing adaptive behaviour
[Fig. 3(c)]. Experiments on rodents have shown that environmental enrichment stimulates neural growth and memory (van Praag et al., 2000). Such effects may be even
more important in fishes where neurogenesis continues throughout life under the
influence of environmental experience (Zupanc, 2008). Marchetti & Nevitt (2003)
found that several brain structures were smaller in size relative to body size in hatchery
fishes than in wild conspecifics, but they could not separate if these effects were
genetic or environmental. Later studies have shown that physical enrichment increases
the 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 only
the size of specific substructures of the brain, being affected by enrichment differs
largely among studies, making it hard to draw conclusions. It should also be mentioned that studies on gross size of the brain, or its substructures, do not provide direct
evidence for increased brain-cell proliferation, as neurogenesis may not reflect itself
as a direct increase in brain size (Lema et al., 2005). Evidence for increased forebrain
cell 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 not
necessarily translate into behavioural differences, but a few studies suggest that this
may indeed be the case (Burns & Rod, 2008; Kotrschal et al., 2013).
Potential mechanisms for the larger brain size and higher brain cell proliferation in
enriched environments could be stimulation of brain growth due to a higher level of
complexity, but it may also be effects of lowered social and environmental stress in the
more complex environment (Sørensen et al., 2013), or it may be side effects of altered
body growth patterns.
Kihslinger & Nevitt (2006) hypothesized that environmental enrichment during an
early critical stage (i.e. the alevin stage) could have lasting effects on neural growth
and proliferation. This hypothesis was not supported in a follow-up study by Näslund
et al. (2012), showing that brain growth in salmonids is plastic. Similar to the study by
Kihslinger & Nevitt (2006), an early effect of enrichment on brain size was found in
S. salar alevins, but the effect gradually disappeared when the developing fry were
moved to conventional rearing tanks. In addition, comparing the brain size of smolts
released into the wild with smolts kept in the hatchery revealed that the latter had
relatively larger brain size, contrary to what is predicted if brain growth is stimulated
by environmental complexity (Näslund et al., 2012). Similar results have been found
when comparing brains of hatchery coho salmon Oncorhynchus kisutch (Walbaum
1792) reared in semi-natural environments with conspecifics from standard hatchery
tanks (Kotrschal et al., 2012). Thus, it appears like releasing hatchery fishes into the
wild may not necessarily lead to stimulation of their brain growth, as the results are
opposite to what are observed when comparing wild with hatchery fishes (Marchetti
& Nevitt, 2003). These counter-intuitive results may potentially be explained by
environment-specific trade-offs between somatic and neural growth.
Growth rate tends to have an effect on the size of neural structures in relation to
the body size, with slow growing fishes having relatively larger brains (Pankhurst
& Montgomery, 1994; Devlin et al., 2012). Part of the explanation for differences
in brain size between wild and hatchery fishes, and between enriched and standard
hatchery-reared fishes, could possibly lay in differences in growth rate, body size and
developmental stage. Hatchery fishes generally have smaller heads in relation to their
bodies than wild conspecifics (Fleming et al., 1994; Vehanen & Huusko, 2011), which
probably 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 smaller
brains. Substructures of the brain grow allometrically in relation to body size, particularly during the alevin and fry stage (Näslund et al., 2012), and slight differences
in size or developmental stage among the compared groups may lead to significant differences in brain structures. There is also allometric change in the brain size during
smolt transformation in salmonids (Ebbesson & Braithwaite, 2012). Further investigations are clearly needed to elucidate the growth trade-offs between body and brain and
head in relation to genetic background and rearing environment, and the effects of such
trade-offs on behaviour.
Learning
Several recent studies support the hypothesis that environmental enrichment can
improve cognitive ability, including learning and general adaptability, to novel conditions [Fig. 3(d)]. For instance, physical enrichment has positive effects on both
neurogenesis and learning in S. salar trained to escape a maze, importantly suggesting
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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 learn
faster in enriched environments than in simple environments (Spence et al., 2011) and
several studies on G. morhua show that in-tank structures increase behavioural flexibility as well as social learning (Braithwaite & Salvanes, 2005; Salvanes & Braithwaite,
2005; Strand et al., 2010). All types of increases in environmental variation are not
necessarily beneficial. For example, Lee & Berejikian (2008) found that enrichment
with stones and plastic plants promoted explorative behaviour in O. mykiss when
tank structures were stable over time. This effect disappeared when structures varied
over time, probably due to stress effects caused by frequent disturbance. Moreover,
environmental enrichment improved foraging efficiency on novel prey in S. salar, but
only if the fish also had previous experience of live food (Sundström & Johnsson,
2001; Brown et al., 2003).
DENSITY REDUCTION
Primarily for economic reasons, captive rearing densities are almost invariably higher
than natural densities. Thus, an obvious effect of most density reductions will be to
make the environment more nature-like which may be generally beneficial to promote
development towards a nature-like phenotype [Brännäs & Johnsson, 2008; Fig. 2(d)].
Although density effects have been well studied in fish farming, research has traditionally been focused on crowding stress, including welfare-associated stress measures
as fin damage and cortisol measurements (Ellis et al., 2002). Altering rearing densities may also have profound influence on behavioural development (Brockmark &
Johnsson, 2010; Brockmark et al., 2010). Some recent progress in behavioural and cognitive research is highlighted to suggest mechanisms through which density may affect
the behaviour of captive fishes. The few empirical studies in which effects of density
on behavioural development have been specifically investigated are also discussed. In
some respects, density can actually be thought of as a form of structure. In fact, in
pelagic environments, schools may provide associated individuals with several advantages resembling those of physical structures, including hydrodynamic savings as well
as shelter from predation (Krause & Ruxton, 2002). Density effects on neural development are still poorly investigated, but may share similarities with the effects induced
by physical enrichment. In addition, density may influence cognition and behaviour
in captive fishes through quite different mechanisms than structure, for example, by
density-mediated effects on social interactions (Sørensen et al., 2013).
Crowding stress
In intensive fish farming, the effects of stocking density have been extensively
studied for a number of traits, but with variable results, suggesting that many factors
interact with density to affect performance in a hatchery (Ellis et al., 2002; Brännäs &
Johnsson, 2008). In several salmonid species, adverse effects of high stocking density
as reductions in survival, food conversion efficiency and growth, as well as increases
in fin damage have been reported (Brännäs et al., 2001; Ellis et al., 2002; Brockmark
et al., 2007). These effects have tentatively been ascribed to stress responses caused
by crowding [Baker & Ayles, 1990; Fig 4(a)]. Some of the negative effects on growth
may be due to reduction of feeding efficiency rather than chronic stress. For example,
increased density can induce scramble competition where individuals simply are
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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J . I . J O H N S S O N E T A L.
getting in the way of each other, increasing losses of food from the hatchery tank
(Ruxton, 1993). Similarly, high density may induce shadow interference, where
individuals experience reduced food intake from being shadowed by competitors
(Elliott, 2002; Krause & Ruxton, 2002). These effects may be more or less severe
depending on how the species in question feed naturally. For example, Arctic charr
Salvelinus alpinus (L. 1758), which is a naturally schooling species, adapt well to
crowding (Brown et al., 1992; Jørgensen & Jobling, 1993). Many flatfish species use
primarily two-dimensional rather than three-dimensional space and rest on the bottom
rather than school. Thus, stocking density of flatfishes is limited by tank bottom
area rather than volume and negative effects on growth performance and survival
have been found in S. solea, (Schram et al., 2006) and Atlantic halibut Hippoglossus
hippoglossus (L. 1758) (Kristiansen et al., 2004). Tank bottom area is also important
in captive rearing of salmonids, as the natural juvenile behaviour of many species is
to reside close to the bottom (Yamagishi, 1962). In gilthead seabream Sparus aurata
L. 1758, high stocking densities increased chronic stress, as indicated by elevation of
plasma cortisol and associated adverse effects on biochemical composition, immune
status and haematology (Montero et al., 1999). Growth rate, however, was not affected
which illustrates the potential problem of relying solely on growth performance as
a 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 goal
as individuals need to be prepared for a post-release environment that is often harsh
and unpredictable (Brännäs & Johnsson, 2008).
Resource defence
Territorial 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 to
decrease with increasing rearing density as the economic defendability of a territory
is inversely related to competitor pressure (Grant, 1997). Consequently, some studies on farmed species such as African sharptooth catfish Clarias gariepinus (Burchell
1822) have found that high densities reduce agonistic behaviour (Kaiser et al., 1995;
Hecht & Uys, 1997). Density effects on competition, however, can be more complex
than just altering aggression levels. In another study on S. alpinus and O. mykiss, using
a self-feeding setup, dominance rank remained unchanged with increasing competitor density, but the relative payoffs of high-ranking individuals decreased (Alanärä &
Brännäs, 1996). There is evidence that hatchery-reared fishes, even when sharing the
same genetic background, are less effective in aggressive contests than wild fishes.
For example, hatchery-reared S. trutta invest more time and energy in territorial conflicts than wild conspecifics without increasing their probability of winning (Deverill
et al., 1999; Sundström et al., 2003). It is not known whether these effects are due to
environmental effects on phenotypic development, or differences in selection intensity
between the hatchery and the natural environment, as discussed previously.
There is, so far, only one study specifically investigating the link between rearing
density, individual competitive ability and post-release performance in the wild
(Brockmark & Johnsson, 2010). The authors found that S. trutta parr reared at natural
density (based on density estimates by Elliott, 1994) had significantly higher dominance rank when competing with fish reared at conventional, and half of conventional
rearing densities. Interestingly, the dominance in low-density trout was due to superior
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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
(a)
Crowding stress
(b)
Resource defence
(c)
Individual recognition
(d)
Individual decision
1959
?
Fig. 4. Potential effects of rearing density in captive environments. (a) High density may increase crowding stress
due 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 ability
to learn and remember individual identities is limited by rearing density, i.e. the number of individuals
encountered. (d) Rearing density may influence the benefits of performing and learning individual behaviour
due to its effects on visual restriction, shadow competition and physical obstruction.
ability to monopolize food rather than overt aggression. Subsequent release into a
stream section with natural predation revealed that the competitive superiority of
low-density S. trutta was translated to increased growth and survival (see Fig. 5;
post-release effects). These results suggest that reduced rearing density facilitates the
development of adaptive behaviour, acquiring life skills that increase post-release fitness. The underlying mechanisms remain speculative. Are the effects due to increased
potential for learned resource defence and contest behaviour at lower densities, or are
there other mechanisms at play as well?
Individual recognition
Environmental effects on social behaviour, as demonstrated above by Brockmark &
Johnsson (2010), may also be mediated by limited attention abilities that constrain the
amount of environmental information that can be processed by animals (Desimone &
Duncan, 1995; Dukas, 2002). Social behaviour is probably facilitated by the development of familiarity with other individuals over time, which in turn is limited by the
number of individual identities that can be learned and memorized, as well as the opportunity 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 develop
social relations with specific individuals, which may impair the development of social
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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J . I . J O H N S S O N E T A L.
Post-release survival (%)
60
40
20
0
0
500
1000
1500
2000
2500
Density (individuals m-2)
Fig. 5. The relation between rearing density and post-release survival in a natural stream section (estimated by
recapture rate) in Salmo trutta parr. Data are based on Brockmark & Johnsson (2010) ( ) and Brockmark
et al. (2010) ( , rearing with added physical structure; , no structure). Fish in both studies were reared
in 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 effects
by dividing the rearing environment to smaller units consistently utilized by a limited
sub-sample of individuals. Previous studies have shown that familiarity can increase
food intake, reduce aggression and increase vigilance towards predation threat in S.
trutta groups, suggesting a link between individual recognition, social competence and
fitness (Höjesjö et al., 1998; Griffiths et al., 2004).
Individual decision
An alternative, not mutually exclusive, explanation suggested by Brockmark et al.
(2010) is that high-density conditions in captivity may alter the trade-off between
using private and public information [Laland, 2004; Brown & Laland, 2011; Fig. 4(d)].
Indeed, human studies show that individuals react to long-time crowding by gradually
reducing 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 for
adaptive decision-making. Thus, high-density conditions that constantly favour the
use of public information over ontogeny might lead to conformity where individuals gradually lose their inherent capacity for independent decision-making. Environmental effects on cognitive and behavioural development, as discussed above, may
help explain the strong density effects on adaptive behaviour (i.e. life skills) found by
Brockmark et al. (2010) where S. trutta parr reared at natural or a fourth of conventional rearing density showed increased ability to feed on novel prey, improved spatial
orientation in a food maze and more efficient anti-predator behaviour, i.e. sheltering in
response to a simulated predator attack. Again, the improved behavioural performance
was mirrored by increased post-release survival in a natural stream section compared
with fish reared at conventional densities (Fig. 5).
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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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 their
phenotypic plasticity and the range of environments to which acclimation is possible
is limited by genetic and developmental constraints (Pigliucci, 2001; Fig. 2). Released
fishes 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 in
other 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 natural
environment before release (so-called soft release) or by improved (i.e. less stressful) transport procedures (Jonsson et al., 1999; Strand & Finstad, 2007). Much of the
post-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 targeted
when aiming to improve rearing methods for stocked fishes.
Enrichment effects
Several 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 increased
estimated sea survival where shelter conditioned fish also dispersed less from the
release point (D’Anna et al., 2012). Enrichment has been found to increase foraging
efficiency in juvenile S. salar (Rodewald et al., 2011) and survival of migrating S.
salar smolts (Hyvärinen & Rodewald, 2013). Moreover, in a recent study by Roberts
et al. (2014), enriched juvenile S. salar had higher recapture rates and occupied more
profitable 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 structures
and water current variability, so their relative importance could not be evaluated. It
should be pointed out that a number of published studies have failed to demonstrate
any 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, enrichment
does not always have ecologically relevant effects and may also be counteracted
by other modifications in the rearing environment. For instance, starvation before
release may increase activity and risk-taking irrespective of prior rearing environment
(Moberg et al., 2011). Other studies also indicate that high rearing densities may
impair and even reverse the positive effects of physical enrichment (Hoelzer, 1987;
Näslund & Johnsson, 2014; unpubl. data).
Density effects
As discussed previously, reduced rearing density appears to facilitate the development of adaptive behaviour in S. trutta parr, resulting in increased post-release survival and growth in their natural stream environment (Brockmark & Johnsson, 2010;
Brockmark et al., 2010). Interestingly, combining the effects of the densities used in
these two studies (which were conducted in the same model system and therefore comparable) suggests that post-release survival is inversely correlated with rearing density
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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over the range of densities used (Fig. 5). The question remains whether these beneficial effects are specific for territorial parr and thereby limited to the freshwater stage of
anadromous salmonids, or are more general, that is, also beneficial for smolt migration
and post-release survival in the sea. Preliminary data support a general effect where
reduced 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 effects
of reduced rearing density on post-release performance are further supported by Barnes
et al. (2013). In their study, post-stocking harvest and spawning returns of landlocked
fall Chinook salmon Oncorhynchus tshawytscha (Walbaum 1792) were consistently
improved by reducing rearing density. Other studies on Pacific salmonids have found
variable effects of rearing density where differences may be attributed to species differences, variation in rearing facilities (e.g. ponds v. raceways) and other sources of
environmental variation (Ewing & Ewing, 1995; Tipping et al., 2004).
CONCLUSIONS
To come back to the first general question asked at the beginning of this paper: is
it feasible to try to mimic key aspects of natural conditions in a full-scale hatchery
to 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 relatively simple environmental modifications of captive environments can significantly
alter phenotypic development of fishes, including effects on neural growth, physiology 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 local
conditions, they can help produce a more wild-like fish with improved post-release
performance. This also partially answers the second question: could studies in artificial
environments such as aquaria or hatchery tanks predict how fishes will perform in the
wild? The short answer is again yes. Several recent studies have shown a link between
adaptive behavioural changes in captivity and post-release performance (Brockmark
et al., 2010). That said, there is still a lack of studies combining laboratory and field
approaches to investigate how phenotypic changes in the captive environment influence post-release fitness, an important challenge for future research. It should also be
stressed that the success of modifications of captive environments has been found to be
highly variable. For example, many studies evaluating physical enrichment have found
no or even negative effects (Näslund & Johnsson, 2014).
To be accepted in full-scale commercial operations, biologically sound modifications of captive environments also need to be economically feasible (Horreo et al.,
2012). For example, reducing rearing densities will increase the production cost per
fish and therefore needs to increase post-release survival and returns of stocked fishes
to meet increased production costs. Similarly, introduction of physical structure in captive environments may increase cleaning costs as well as the risk of infections. In many
countries, however, there is a growing public concern, as well as increasingly strict legislation concerning animal welfare where the ultimate goal is to minimize stress and
allow natural behaviour to be expressed, the latter goal being the more important one
for stocked fishes.
© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971
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In summary, it can be concluded that both physical enrichment and reduced density have potential to increase the fitness of hatchery fishes released into natural
environments, but the success of these manipulations is strongly dependent on
adequately adapting methods to species and life stage-specific conditions. Further
development of rearing methods for fishes to be released in the wild should be based
on research applying state-of-the art biological knowledge in a multidisciplinary
framework including economical and societal aspects.
This study was funded by the strategic project SMOLTPRO, financed by the Swedish Research
Council Formas. We thank C. Garcia de Leaniz and an anonymous reviewer for helpful comments on the manuscript.
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© 2014 The Fisheries Society of the British Isles, Journal of Fish Biology 2014, 85, 1946–1971