ArticlePDF Available

Environmental enrichment for fish in captive environments: Effects of physical structures and substrates


Abstract and Figures

Structural environmental enrichment, that is, a deliberate addition of physical complexity to the rearing environment, is sometimes utilized to reduce the expression of the undesirable traits that fish develop in captivity. Increasing demands and regulations regarding usage of enrichment to promote fish welfare also make investigations on the effects of enrichment important. Here, we sythesize the current state-of-the-art knowledge about the effects of structural environmental enrichment for fish in captive environments. We find that enrichment can affect several aspects of the biology of captive fish, for example, aggression, stress, energy expenditure, injury and disease susceptibility. Importantly, these effects are often varying in direction and magnitude, and it is clear that just addition of structure is not a solution to all problems in fish rearing. Each species and life stage needs special consideration with respect to its natural history and preferences. A multitude of different enrichment types has been investigated and many studies investigate several enrichment components at the same time, making comparisons among studies difficult. To the present date, the majority of efforts have been directed to investigate salmonid fish in stock-fish hatcheries and cichlids from a basic research perspective. Some contexts are under-studied with respect to environmental enrichment, for instance effects on results in basic research and welfare effects in display aquaria. There are many research opportunities left within this field. However, future studies could utilize experimental designs which make it possible to discriminate between effects of different environmental manipulations to a higher degree than what has been performed to this date.
Content may be subject to copyright.
Environmental enrichment for sh in captive environments:
effects of physical structures and substrates
Joacim N
aslund & J
orgen I Johnsson
Department of Biological and Environmental Sciences,University of Gothenburg,Gothenburg,Sweden
Structural environmental enrichment, that is, a deliberate addition of physical com-
plexity to the rearing environment, is sometimes utilized to reduce the expression
of the undesirable traits that fish develop in captivity. Increasing demands and reg-
ulations regarding usage of enrichment to promote fish welfare also make investi-
gations on the effects of enrichment important. Here, we sythesize the current
state-of-the-art knowledge about the effects of structural environmental enrichment
for fish in captive environments. We find that enrichment can affect several aspects
of the biology of captive fish, for example, aggression, stress, energy expenditure,
injury and disease susceptibility. Importantly, these effects are often varying in
direction and magnitude, and it is clear that just addition of structure is not a solu-
tion to all problems in fish rearing. Each species and life stage needs special consid-
eration with respect to its natural history and preferences. A multitude of different
enrichment types has been investigated and many studies investigate several
enrichment components at the same time, making comparisons among studies diffi-
cult. To the present date, the majority of efforts have been directed to investigate
salmonid fish in stock-fish hatcheries and cichlids from a basic research perspective.
Some contexts are under-studied with respect to environmental enrichment, for
instance effects on results in basic research and welfare effects in display aquaria.
There are many research opportunities left within this field. However, future stud-
ies could utilize experimental designs which make it possible to discriminate
between effects of different environmental manipulations to a higher degree than
what has been performed to this date.
Keywords Aquaculture, aquarium, environmental complexity, environmental
enrichment, fish husbandry, welfare
Joacim N
Department of
Biological and
Sciences, University
of Gothenburg, Box
463, Gothenburg,
SE-405 30, Sweden
Tel.: +46317863696
+46 31 41 67 29
E-mail: joacim.
Received 13 Apr
Accepted 25 Jun
Introduction 2
Background 2
Aims and methods 3
Definition of environmental enrichment 3
Goals of environmental enrichment programs for sh 4
Welfare 4
Food production 5
Fisheries and conservation management 5
Research 6
©2014 John Wiley & Sons Ltd DOI: 10.1111/faf.12088 1
F I S H and F I S H E R I E S , 2016, 17, 1–30
Display aquaria 6
Ecological relevance of structural complexity 6
Effects of structural enrichment 7
Structures as shelters 7
Structures for reduction of aggression 9
Structures for sensory and cognitive stimulation 10
Structures inducing environmental variability and unpredictability 11
Tank floor substrates 11
Incubation substrates 12
Toys 13
Physical structures in combination with other types of enrichment 14
Structures in periphyton-based aquaculture 14
Treatments closely related to structural enrichment 14
Tank cover 14
Pond rearing 15
Potential problems with environmental enrichment 16
Post-release effects: do enriched sh perform better? 16
Preferences: what do the shes actually want? 17
General considerations for environmental enrichment research in sh 17
Concluding remarks 18
Acknowledgements 19
References 19
Supporting Information 30
‘[...] the smooth sides and bottoms of the troughs
are not conductive to fostering their hiding pro-
clivities and this soon becomes weakened; to
counteract this somewhat I placed a layer of fine
gravel in the bottom of all the troughs last season,
with good results’.A. Robertson, 1919
Fish are reared in captivity for a number of differ-
ent reasons, for example, food production, conser-
vation, stock enhancement, stocking for angling,
research and as ornamentals (Huntingford et al.
2012). The differences between artificially reared
and wild fish have been a recurring subject in fish
biology over the past century and considerable evi-
dence has now accumulated that fish reared in
artificial environments deviate from wild fish (e.g.
Schuck 1948; Blaxter 1970; Olla et al. 1998; Met-
calfe et al. 2003; Chittenden et al. 2010). Life in
captivity generally promotes traits other than
those adaptive in the wild, which also may lead to
rapid selection for domestic genotypes, sometimes
within a single generation (e.g. Vincent 1960;
Metcalfe et al. 2003; Christie et al. 2012).
Fish culturists and researchers have discussed
and tried out a variety of methods to avoid devel-
opment of maladaptive or unwanted traits in cap-
tive fish, especially when they are destined for
release into nature (Flagg and Nash 1999; CHSRG
- California Hatchery Scientific Review Group
2012), but also when fish are used as model
organisms in laboratories (Williams et al. 2009).
In addition, there is a rising public concern for the
welfare of captive fish (Huntingford et al. 2006).
Environmental enrichment (hereafter ‘EE’) is one
suggested strategy for coping with all these issues.
National and international legislation and guide-
lines for fish are becoming increasingly detailed
and do often recognize that EE may be required to
satisfy goals of sufficient welfare (CCAC 2005; Jo-
hansen et al. 2005; Council of Europe, 2006;
NRCNA 2011). Along with such regulations fol-
lows a requirement to understand how different
rearing environments affect fish. Furthermore, it is
important to investigate how different types of EE
affect food and stock-fish production, as well as
the results of basic research involving fish as
2©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
experimental subjects. Here, we summarize and
synthesize the results of research conducted within
the field of EE for fish in captive environments
(food aquaculture, stocking programmes, public or
private aquaria and research facilities).
Aims and methods
Our aim is to provide a state-of-the-art synthesis of
the effects of structural EE (see definition below).
The synthesis is based on a systematic summary
of published literature (see Table S1S3, electronic
supplement), with literature searches being con-
ducted through extensive keyword searches in
research paper databases (Google Scholar,Web of
Knowledge and Scopus; all with differing advantages
and limits (Falagas et al. 2008)), as well as by
tracking literature from reference lists. The inten-
tion is to cover the published literature as com-
pletely as possible, but a few papers may have
been overlooked. A summary of the number of
enrichment studies conducted for different orders
of fish is presented in Fig. 1.
To evaluate the extent to which EE is used in
the current research in fish biology, we conducted
a survey of the use of structural EE in experimen-
tal setups. For this survey, we read the methods
sections in papers (original articles and short com-
munications) describing experiments on captive
fish, published in Journal of Fish Biology,Transac-
tions of the American Fisheries Society,Environmental
Biology of Fishes and Fish Physiology and Biochem-
istry. These journals were chosen as they are
specialized on fish research and publish a high
proportion of laboratory studies. Years (2003,
2008 and 2013) were chosen to give an overview
of the last decade. We surveyed four issues for
each journal and year, except for Fish Physiol. Bio-
chem. in 2013, where only two issues were cov-
ered, due to increased numbers of papers per
issue. Results from the survey are presented in
Fig. 2.
Definition of environmental enrichment
We define EE in general as a deliberate increase in
environmental complexity with the aim to reduce mal-
adaptive and aberrant traits in fish reared in otherwise
stimuli-deprived environments. Traits could be physi-
ological, behavioural, morphological and psycho-
logical and considered maladaptive with respect to
fitness components (health, survival, reproduction,
etc.). Aberrant traits, such as stereotypies, are
often unwanted, for example, in public or private
aquaria and research facilities, even if they do not
directly affect the fitness of the individual fish.
Some enrichment strategies might not work in the
intended way, but they are still enrichments
according to our definition as they still increase
the complexity in the rearing environment. Thus,
an EE study was not required to result in desired
outcomes to be included in our synthesis. Other
Physical structures and substrates Periphyton substrates
Perciform es
Atheri niformes
Perciform es
Figure 1 Number of papers investigating effects of environmental enrichment (structures or substrates) published for
different orders of fishes. Lists of the papers on which the figure is based are found in the electronic supplement (Tables
S1, S2 and S3).
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 3
Structural enrichment for captive fish JN
aslund and J I Johnsson
alterations of the environment, for example,
increasing water quality or adding nutrients to the
feed, are not considered as EE here. Other authors
have presented different definitions of EE with
more restrictive or general terms and goals (e.g.
Shepherdson 1994, 2003; Newberry 1995; Shep-
herdson et al. 1998; Mellen and Sevenich Mac-
Phee 2001; Westlund 2014).
Environmental enrichment is often divided into
different categories, depending on the goals of the
enrichment programme (e.g. Young 2003). Com-
monly recognized categories are: (i) physical enrich-
ment, including modifications or additions to the
tanks, that is, structural complexity; (ii) sensory
enrichment, which concerns stimulation of the sen-
sory organs and the brain; (iii) dietary enrichment,
encompassing type and delivery of food (note the
distinction from nutrient enrichment, which con-
cerns addition of nutrients to the feed); (iv) social
enrichment, adding contact and interactions with
conspecifics; and (v) occupational enrichment, relat-
ing to reduction of physical and psychological
monotony by introducing variation to the environ-
ment and possibilities for exercise and performance
of preferred behaviours. Giving animals the possi-
bility to choose their environment may be benefi-
cial as it increases their control (e.g. they can
choose to avoid certain aggressive conspecifics),
but conclusive evidence that choice in itself is ben-
eficial is lacking (Hutchinson 2005). We focus on
physical enrichment through addition of structures
and substrates into the rearing environment.
Goals of environmental enrichment
programmes for sh
Setting specific goals for EE programmes is of pro-
found importance (Mellen and Sevenich MacPhee
2001; Young 2003) as the usage of environmen-
tal enrichment can have different aims. In the fol-
lowing section, we shortly present general goals of
enrichment applications for animal welfare, fisher-
ies management, food production, research and
display aquaria.
Following Huntingford et al. (2006, 2012), fish
welfare can be approached from three different
angles: functions-, feelings- and nature-based,
which may be more or less appropriate depending
on context. Importantly, different indicators of
poor welfare are not always in line with each
other (Huntingford et al. 2012). Objective compar-
isons among the approaches are difficult, if not
impossible, as much information about fish percep-
tion and cognition is lacking. Comparisons are
also complicated by the fact that there are sub-
stantial differences in what is considered appropri-
ate animal welfare among human cultures
(Turnbull and Kadri 2007).
In the functions-based view, appropriate welfare
means that the fish is able to adapt physiologically
to its captive environment and maintain its biolog-
ical systems in function. This is probably the most
commonly used welfare concept in food production
aquaculture, as it is easy to get direct measures
of welfare using productivity-based assessment
(i.e. by monitoring mortality and growth rates) or
from a wide suite of physiological parameters
relating to allostasis (Iwama 2007; Segner et al.
2012). However, when it comes to conservational
aquaculture where assessments are often based on
post-release welfare, measures taken in captivity
% of papers
No/not specified
Journal of Fish Bilology. 2003
Journal of Fish Bilology. 2013
Transactions of the American Fisheries Society. 2003
Transactions of the American Fisheries Society. 2008
Transactions of the American Fisheries Society. 2013
Environmental Biology of Fishes. 2003
Environmental Biology of Fishes. 2008
Environmental Biology of Fishes. 2013
Fish Physiology and Biochemistry. 2013
Fish Physiology and Biochemistry. 2003
Fish Physiology and Biochemistry. 2008
Journal of Fish Bilology. 2008
26 31 13 12 10 7 6 7 26 41 43
Figure 2 Percentage of papers reporting on usage of
environmental enrichment in studies involving captive
held fish from four scientific journals specialized on fish
research (Journal of Fish Biology, Transactions of the
American Fisheries Society, Environmental Biology of
Fishes and Fish Physiology and Biochemistry). Numbers
above pillars show number of papers included in the
survey. The vast majority of papers included in the ‘No/
Not specified’ category did not explicitly state that the
rearing environment was barren.
4©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
may be less important or even poor indicators of
successful rearing strategies as performance in
captivity may be uncorrelated or even negatively
correlated with performance in the wild (Saikko-
nen et al. 2011; Bergman et al. 2013).
Within the feelings-based concept (also called
the affective state view), the main concerns are
the fishes’ emotional experiences in the rearing
environment. To approach good welfare, the aims
should be to minimize negative stimuli and maxi-
mize positive stimuli. Within this concept, it is
assumed that fish are able to have negative and
positive experiences. Several studies suggest that
fish can experience pain-, fear-, frustration- or
anxiety-like feelings (Broom 1998; Maximino et al.
2010; Vindas et al. 2012; Braithwaite 2014), but
whether or not they are suffering is subject to an
extended scientific debate (see e.g. Braithwaite
2010; Rose et al. 2014). Physiological parameters
are less useful within this approach, because we
do not know how alterations of the physiological
systems are reflected in the subjective feelings of a
fish (Iwama 2007; Lund et al. 2007). Feelings of
fishes can merely be evaluated by indirect infer-
ence from behaviour (Lund et al. 2007; Hunting-
ford et al. 2012; Martins et al. 2012) or by
preference-based valuation (Volpato et al. 2007).
Nevertheless, feelings-based welfare is probably the
most important approach for people concerned
about animal welfare and rights (Lund et al.
2007; Lindstr
om 2008; Huntingford et al. 2012).
In public aquaria, any behaviour that can be asso-
ciated with reduced feelings-based welfare by
humans, whether negatively experienced or not by
the fish, are unwanted (Scott et al. 1998; Smith
2006). If fish have the ability to experience dis-
comfort in typical captive environments, this may
also influence research based on fish models, as it
may influence the validity of attained results. EE
that reduces stereotypic or otherwise odd behav-
iours, for instance, structures that keep fish occu-
pied in their tanks, could be assumed to have
beneficial effects within the feelings-based
According to the nature-based approach, the
fish should have a ‘natural’ life, which as fully as
possible allow performance of natural behaviour.
This often conflicts with the other welfare concepts
since some disturbance (e.g. the stress experienced
when being chased by a predator) is natural and
adaptive, and as all restrictions to natural behav-
iour do not necessarily affect function or feelings
(Huntingford et al. 2012). Some natural behaviour
is also directly reducing general welfare in the
tanks, for example conspecific aggression. The nat-
ure-based concept is probably most useful when
conditioning fish for release into the wild, but less
so for domesticated fish which are likely not
adapted for ‘natural’ conditions due to domestica-
tion selection (Newberry 1995). Typical nature-
based approaches attempt to make the environ-
ment more nature-like, for example by introducing
structural complexity, temporal environmental
variation or live food.
Regardless of which of the above concepts that
is adopted, appropriate handling of fish welfare
issues requires interactions between science and
ethics, incorporating both empirical research and
normative moral theories on the relevance of fish
capacities (Bovenkerk and Meijboom 2012).
Food production
In food production aquaculture, the goals of EE
are related to economics and the ethical profiles of
companies. Increased yield could be reached if EE
leads to increased survival, facilitates increased
stocking density, or contributes to increased
growth or quality. Increasing welfare may also
have economic benefits, either directly by higher
acceptance to buy cultured fish, or indirectly by
improved appearance of the fish (e.g. reduced inju-
ries or fin damage) (Olesen et al. 2010; Grimsrud
et al. 2013). However, such economic gains can
be uncertain due to gaps between ethical attitudes
and actual consumer behaviour (Carrigan and At-
talla 2001). In addition, there are concerns that
some aspects of fish welfare are compromised in
modern aquaculture due to economic interests
(Bergqvist and Gunnarsson 2011).
Fisheries and conservation management
Stocking has been an important tool for fisheries
managers for more than a century (e.g. Kerr
2006), but hatchery fish are often ill suited for a
life in the wild (e.g. Olla et al. 1998; Cowx 1999;
Einum and Fleming 2001; Araki et al. 2008).
Morphological and behavioural differences
between wild and hatchery-reared fish are known
since long (e.g. S
orensen 1919; Robertson 1919;
Vincent 1960; Kellison et al. 2000; Sundstr
et al. 2004; Vehanen and Huusko 2011) and indi-
viduals doing well in captivity are not necessarily
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 5
Structural enrichment for captive fish JN
aslund and J I Johnsson
the same ones doing well in nature (Vincent
1960; Saikkonen et al. 2011). Thus, if EE can
result in more nature-like fish, it could be part of
responsible stock-enhancement programmes, for
example, as a preconditioning strategy, or in opti-
mizing rearing processes and release strategies
(e.g. Lorenzen et al. 2010). In addition, nature-like
morphology of stock-fish, particularly absence of
fin damage, is valued by anglers (Sternberg 1988).
For any animals destined for release (e.g. in stock
enhancement, re-stocking, supplementation, intro-
duction, or sea ranching programs), modifications
of the captive environment to resemble the release
habitat could be of high importance (Newberry
1995). The concept of life-skills training, where
fish are given opportunity to learn natural behav-
iours typical for their species, has been suggested
and investigated, with some promising results
involving EE (Suboski and Templeton 1989;
Brown and Laland 2001). Life-skills training is clo-
sely connected to the nature-based welfare con-
cept. EE-induced nature-like phenotypes could be
potentially beneficial to the fish after release, even
if some aspects of functions- or feelings-based wel-
fare are compromised in the captive environment
due to the EE itself. Furthermore, calls for quality-
based stocking policies, rather than quantity-
based, have been made repeatedly (e.g. Anders
1998; CHSRG 2012). From this view-point, it is
important to consider the cost per surviving fish,
instead of cost per released fish. If EE can improve
survival, less fish needs to be reared for stocking.
In fish research programmes where experiments
are conducted using captive fish as model organ-
isms, consideration of the rearing environment
can be of great importance for the validity of
results (Killen et al. 2013). Thus, the aim of EE in
research environments is to produce reliable and
relevant measurements of the variables under
investigation (Williams et al. 2009). However,
every environmental factor could influence results
in different ways, with both masking and enhanc-
ing effects, and such effects can be species specific
(Killen et al. 2013). To be able to optimize the
environment for the aims of a research pro-
gramme, there is need for careful, evidence-based
evaluation of EE strategies prior to conducting the
research (Benefiel et al. 2005; Williams et al.
Display aquaria
Display aquaria have, since the beginning of the
practice, been constructed for mainly educational
and recreational purposes, but also with some sci-
entific and conservational aims (Seal 1890; Hutch-
ins et al. 2003). Accordingly, the goal of EE in
public and private aquaria is partly to promote
welfare and natural behaviours, but also to attract
the fish to certain areas of the tank where they
are more visible (Smith 2006; Goosen et al. 2008;
Kato et al. 2010; Costa et al. 2011). An additional
aim is to construct an environment that in itself is
aesthetically appealing for a human beholder.
Thereby, the usage of enrichments in aquaria is
often a compromise between what is beneficial for
the fish and appealing to the owner (Sj
and Wickman 1976).
Ecological relevance of structural complexity
Structural complexity is an important factor in
many aquatic ecosystems. Some fish species are
pelagic throughout their lives, but most have at
least some connection (e.g. foraging, sheltering or
spawning) with solid structures at some life stage
(Nikolsky 1963). Environmental complexity, made
up of physical structures (stones, roots, logs,
plants, algae, sand, sessile animals, ice, artificial
objects etc.) is thus an important environmental
factor in the natural environment of many spe-
cies. An obvious function of complexity is to pro-
vide shelter; either to evade actively hunting
predators (Angermeier and Karr 1984; Morice
et al. 2013), or to escape hydraulic forces such as
strong currents (Allouche 2002). Shelter may
also be used by predators to successfully ambush
their prey (Skov and Koed 2004). In territorial
animals, increased environmental complexity has
been shown to reduce aggression and territory
size, allowing more individuals per unit area (Kal-
leberg 1958; Eason and Stamps 1992; Grant
1997; Dolinsek et al. 2007b; Gustafsson et al.
2012). The mechanisms behind this are probably
reduced visual contact among dominant individuals
and increased cost of territory defence (Eason and
Stamps 1992; Dolinsek et al. 2007a). Increased
complexity also creates refuges for subordinate
individuals (H
oet al. 2004). Complexity may
also affect foraging rate, either negatively due to
decreased activity from sheltering, lowered
manoeuvrability or reduced prey detectability
6©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
(reviewed in Gotceitas and Colgan 1989), or posi-
tively due to modification of innate predator
avoidance behaviours in protected complex envi-
ronments (Allen-Ankins et al. 2012) and accumu-
lation of prey organisms (Gustafsson et al. 2014).
Generally, negative effects tend to be more com-
mon (Gotceitas and Colgan 1989). Effects on ter-
ritoriality and foraging are likely to affect growth
rate, but there are also some indications that
complexity may also affect the allometry of
growth, altering the phenotype expression (Gar-
no-Paz et al. 2010). During the reproductive
period, many species uses structures as nests or
nest materials (Nikolsky 1963), and environmen-
tal complexity may alter the mating behaviour
(Olla et al. 1981; Candolin and Voigt 1998; My-
hre et al. 2013). Many of the species kept in arti-
ficial rearing environments are naturally adapted
to live in close association with structures and
the presence or absence of structures may impact
their growth, behaviour, physiology and overall
welfare. Different kinds of structures can have dif-
ferent effects, which also may be specific depend-
ing on the ecology of the species in question.
Effects are, however, not necessarily only species
specific, but may also be specific for populations
or even individuals, a detail which become more
and more evident from ‘animal personality’
research within the fields of behavioural ecology
and physiology (Conrad et al. 2011; Koene
2013). Utilization of structures may also depend
on time of day (Shoup et al. 2003) or season
(Valdimarsson and Metcalfe 1998) and may also
change during ontogeny (Werner and Hall
In the following section, we present summaries
of effects of structural enrichment on fish in
captivity. The results are structured under differ-
ent sections depending on the aim of the EE pro-
vided. However, effects are often overlapping
across contexts, as structural enrichment may
serve several functions, for example, both as shel-
ter and as vision-limiting topology. Thus, our cat-
egorization of effects mainly serves as a guide for
the reader.
Effects of structural enrichment
Structures as shelters
In fish-rearing environments, structural enrich-
ment can be added with an aim to mitigate
environmental stressors, such as human activity
or intraspecific aggression. Added shelters are
indeed often utilized by the captive fish, at least in
species which typically uses shelters in their natu-
ral environment (e.g. Brown et al. 1970; Slav
et al. 2012; Santos et al. 2013). A study on
Atlantic salmon even suggests that the mere pres-
ence of a shelter (i.e. not necessarily the utiliza-
tion of it) has beneficial effects, leading to reduced
basal metabolic rate (Millidine et al. 2006). Shelter
deprivation has been shown to cause distress in
vipers (Bonnet et al. 2013), which utilize shelters
as part of their natural behaviour; the same could
be true in fish, leading to increased energy expen-
Two types of shelters are typically used for fish,
either cover structures like pipes, tiles and non-
buoyant plastic strips, or structures inhibiting
manoeuvrability like entangled plastic strips or net
structures. The former type is typically used to
provide hiding places, while the latter is used to
inhibit cannibalism and aggressive behaviour.
In aquaculture, provision of shelter structures
has been shown to have beneficial effects in sev-
eral species of catfish, which are naturally adapted
for a life on the bottom and are often nocturnal,
spending the light hours in cover. Growth and
survival was improved in net pen culture of smal-
ler sizes of juvenile vundu catfish Heterobranchus
longifilis (Clariidae), where cannibalism is usually
high (Coulibaly et al. 2007). Cannibalism was,
however, not reduced when providing shelters in
aquaria for the same species (Baras et al. 1999).
The differing results could depend on the fact that
shelter structures where different between the
studies (entangled plastic strips in the former, half
PVC cylinders in the latter), as well as number of
fish, experimental time and rearing environment.
Shelter structures (plastic mesh materials) reduced
cannibalism in African sharptooth catfish Clarias
gariepinus (Clariidae) (Hecht and Appelbaum
1988; Hossain et al. 1998), but not in juvenile
Asian redtail catfish Hemibargus nemurus (Bagri-
dae) (Rahmah et al. 2013). The function of shelter
as light refuge in nocturnal sharptooth catfish has
also been indicated, as growth in constantly lit
tanks was enhanced with the addition of shelter,
while no effect was observed in constantly dark
tanks (Britz and Pienaar 1992). Shelters have also
been shown to reduce stress (as indicated by
plasma concentrations of the stress hormone corti-
sol) in South American catfish Rhamdia quelen
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 7
Structural enrichment for captive fish JN
aslund and J I Johnsson
(Heptapteridae), if combined with darker (blue)
tank colour (Barcellos et al. 2009).
Shelters also reduced the basal plasma cortisol
levels in Atlantic salmon Salmo salar (Salmoni-
dae), an effect that is hypothesized to be due to
reduced impact of intermittent stressors and con-
specific aggression (N
aslund et al. 2013). The
presence of shelter may have led to the avoidance
of aggressive individuals, as the level of fin deteri-
oration was lowered compared with barren tanks
aslund et al. 2013). Reduced fin damage in
enriched environments has been observed also in
other salmonid species such as cutthroat trout
Oncorhynchus clarkii (Salmonidae) and rainbow
trout Oncorhynchus mykiss (Salmonidae) (Bosa-
kowski and Wagner 1995; Wagner et al. 1995;
Arndt et al. 2001; Berejikian and Tezak 2005);
however, reductions in fin deterioration may also
depend on reduced abrasion with the environ-
Increased propensity for sheltering in novel
environments is demonstrated in Atlantic cod Ga-
dus morhua (Gadidae), Atlantic salmon, and white
seabream Diplodus sargus (Sparidae) reared with
shelter structures (Salvanes and Braithwaite 2005;
Roberts et al. 2011; D’Anna et al. 2012; N
et al. 2013). Such behaviour is likely beneficial if
the fish are to be released into natural waters, as
indicated by the increased sea survival in the shel-
ter-reared sea bream (D’Anna et al. 2012). How-
ever, effects may vary depending on species and
release environment (see section Post-release effects
Rearing environments with artificial vegetation
reduce the startling response in pike Esox spp.
(Esocidae) (Einfalt et al. 2013) and also reduce
adaptation time to experimental conditions and
shoaling behaviour in common bream Abramis
brama (Cyprinidae) (Gerasimov and Stolbunov
2007). In Atlantic cod, EE leads to reduced swim-
ming activity and more context-dependent vari-
ability in shoaling (Salvanes and Braithwaite
2005; Salvanes et al. 2007; Moberg et al. 2011).
Activity has also been shown to decrease in zebra-
fish Danio rerio (Cyprinidae) provided with gravel
and plants, as compared to barren-reared fish (von
Krogh et al. 2010).
Cod provided with cover spent less time interact-
ing with frayed parts of their net cage, which
could reduce the probability of escape from in-sea
cod farms (Zimmermann et al. 2012). In the ben-
thic burbot Lota lota (Gadidae), more fish sheltered
when a larger number of shelters was introduced
in the rearing tanks, resulting in overall reduced
swimming activity (Wocher et al. 2011). Concor-
dantly, in another study on burbot, metabolism
was substantially reduced when appropriate shel-
ter structures (cobble) were added to tanks (Fi-
scher 2000). In contrast, metabolism was not
significantly affected by providing shelters in a
complementary study on stone loach Barbatula
barbatula (Nemacheilidae), which also is a benthic
species, showing that results cannot be generalized
even among species with similar ecology (Fischer
Effects on growth seem to depend on species
and the size of the fish, which probably reflects the
ecology of the species in question. Several studies
on salmonids indicate negative effects (Bosakowski
and Wagner 1995; Wagner et al. 1996; Maynard
et al. 2004; Lema et al. 2005; Fast et al. 2008),
others show no effects (Arndt et al. 2001; Brock-
mark et al. 2010; Roberts et al. 2011; N
et al. 2013), and a few point to positive effects
(Brockmark et al. 2007; Hyv
arinen et al. 2011).
In catfishes (Siluriformes), there are several indica-
tions of positive effects, but they seem to be depen-
dent of the size of the fish and environmental light
levels (Britz and Pienaar 1992; Hossain et al.
1998; Coulibaly et al. 2007; Rahmah et al. 2013).
Positive effects on growth have also been shown
in zebrafish (Spence et al. 2011; Langen 2012),
mud eel Monopterus cuchia (Synbranchidae) (Nare-
jo et al. 2003), European eel Anguilla anguilla (An-
guillidae) (Kushnirov and Degani 1991), and
European minnow Phoxinus phoxinus (Cyprinidae)
(Wootton et al. 2006), while no effects were
observed for three-spined stickleback Gasterosteus
aculeatus (Gasterosteidae) (Wootton et al. 2006),
pikes (Einfalt et al. 2013) and sleepy cod Oxyeleo-
tris lineolata (Eleotridae) (Herbert et al. 2003),
although the latter species did increase in condi-
tion factor when shelters were present.
In conclusion, effects of shelters largely depend
on species and what kinds of shelters are used. In
general, cover structures reduces activity and
potentially save energy through decreased metabo-
lism and reduced stress. However, spending less
energy does not necessarily lead to improved
growth rates, as increased sheltering may reduce
time spent foraging. Structures may also reduce
the detectability of food provided in the tank.
Shelters may also lead the fish to learn adaptive
antipredator behaviour, which could be valuable
8©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
in fish stocked for conservation purposes. Effects
could potentially be less pronounced in domesti-
cated fish as these may have been selected for
reduced desire to shelter, as selection for rapid
growth is likely to increase foraging activity as
well (Vincent 1960; Johnsson 1993).
Structures for the reduction of aggression
Theoretical and empirical work suggests that terri-
toriality, and hence related aggression, is depen-
dent on several factors like activity, food
availability, competitor density and detectability of
intruders (Schoener 1987; Eason and Stamps
1992; Grant 1997). Thus, introduction of physical
structure in captive environments can potentially
reduce aggression by restricting visual contact and
reduce general activity levels. In salmonid hatch-
eries, for example, structural enrichment can
reduce dorsal fin damage (see Table S1), which
may be due to reduced aggression levels from
visual isolation and/or increased sheltering oppor-
tunities for subordinates, as noted previously.
Direct measures of reduced aggression in struc-
tured tanks have been observed for salmonids
(Mork et al. 1999), but not in all cases (Riley et al
09). Reductions in agonistic interactions have also
been observed in other species (zebrafish: Basquill
and Grant 1998; Carfagnini et al. 2009; Wilkes
et al. 2012, spotted wolfish Anarhichas minor (An-
arhichadidae): Lachance et al. 2010, pearl cichlid
Geophagus brasiliensis (Cichlidae): Kadry and Bar-
reto 2010 and Midas cichlid Amphilophus cf. citrin-
ellus (Cichlidae): Oldfield 2011). However,
aggression appears to be dependent on the level of
complexity. If the density of structural objects is
high, the enrichment is likely to reduce aggression
due to reduced encounter rate and limited field of
sight (Eason and Stamps 1992). If structures are
too limited in numbers in relation to fish density,
there may instead be an increase in aggression
from competition for access to the structures. This
effect has been observed in Eurasian perch Perca
fluviatilis (Percidae), black seabass Centropristis stri-
ata (Serranidae) juveniles and gopher rockfish
Sebastes carnatus (Sebastidae) (Hoelzer 1987; Gwak
2003; Mikheev et al. 2005). In the black sea bass,
the increased aggression also led to reduced sur-
vival and growth of the experimental fish (Gwak
2003). In courtship trials, butterfly splitfin Ameca
splendens (Goodeiidae) males increased aggression
when EE was present, indicating that the
enrichment was considered as a defendable
resource by this species as well (Kelley et al. 2006).
Barreto et al. (2011) concluded that structural EE
was negatively affecting Nile tilapia Oreochromis
niloticus (Cichlidae) as it increased aggression, but
in this study only a single, low level of complexity
was investigated. Possibly, more structures could
have reduced aggression. As an example, when
comparing two levels of structural complexity, Bar-
ley and Coleman (2010) found that convict cich-
lids Amatitlania nigrofasciata (Cichlidae) were less
aggressive when more structures were available. In
redbreast tilapia Tilapia rendalli (Cichlidae), the
latency to initiate aggressive interactions was
decreased in structured environments but the
number of attacks was also reduced (Torrezani
et al. 2013). This suggests that structures can be
considered to be defendable resources, but when
the subordinate is not intruding into the defended
area anymore, the conflict settles. Thus, structures
may help to delimit territories which subordinates
then can avoid to minimize risk of getting injured.
The discrepancy between results from the Nile tila-
pia and readbreast tilapia studies could potentially
depend on species differences in territory size in
relation to tank size. Tank size, as well as EE, does
indeed affect agonistic behaviours in Midas cichlids
(Oldfield 2011).
Increased aggression may also be a result of dis-
tress, or lack of occupation in the tanks. Batzina
et al. (2014a,b,c) provided gilthead seabream Spa-
rus aurata (Sparidae) with gravel substrate with
which the fish could interact (e.g. search for food),
and this led to lower activity of brain monoamines
and reductions in agonistic behaviours among
their fish. However, effects were only apparent
when using certain colours of gravel, with blue
gravel giving most pronounced effects (Batzina &
Karakatsouli 2012; Batzina et al 2014b).
Summing up the studies on aggression in rela-
tion to EE, additions of physical structures are
expected to affect the levels of aggression in the
tanks. The effects, however, are likely to be species
specific and also dependent on the level of com-
plexity added. In some cases, for instance, when
too few structures are added, there may be
increased aggression due to defence of the
structures. In other cases, reduction in aggression
is likely. It is thus of profound importance to adapt
EE solutions carefully to the biology of the species
in question as well as to control that the intended
effects really are achieved.
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 9
Structural enrichment for captive fish JN
aslund and J I Johnsson
Structures for sensory and cognitive stimulation
Natural environments are full of sensory stimuli.
In contrast, artificial rearing facilities are often
much less variable and tank reared fish are
thereby potentially deprived of sufficient input for
proper development of sense organs (Blaxter
1970). Additions of structures to the captive envi-
ronment have thus often been used with the aim
of stimulating sensory and cognitive development
(Sackett et al. 1999). For instance, suppression of
visual input by rearing fish larvae in darkness will
affect the brain (specifically the optic tectum) in
fish (Pflugfelder 1952). Structural complexity also
provides visual complexity. Thus, structural
enrichment could also be visual enrichment if the
complexity is sufficient.
Recent studies show that more complex envi-
ronments stimulate cell proliferation and can
increase the cognitive ability of fish. A study in
zebrafish showed that rearing for a week in
enriched environment increased brain cell prolifer-
ation in the forebrain (telencephalon, where the
main cognitive centre are thought to be located),
as indicated by proliferating cell nuclear antigen
(PCNA) immunohistochemistry (von Krogh et al.
2010). Furthermore, Atlantic salmon reared in EE
had increased telencephalic expression of the
transcription factor neurogenic differentiation 1
(NeuroD1), an indicator of neurogenesis (Salvanes
et al. 2013). However, Lema et al. (2005) have
presented results showing possible negative effects
of EE on neurogenesis for juvenile coho salmon
Oncorhynchus kisutch (Salmonidae), based on BrdU
staining of telencephalic regions. Other studies
has shown that the growth of the brain, or differ-
ent substructures of the brain, relative to the
body, could be affected by EE (Kihslinger and Ne-
vitt 2006; Kihslinger et al. 2006; N
aslund et al.
2012; but see Burns et al. 2009). Consequently,
Kihslinger et al. (2006) suggested that early expo-
sure to a complex environment during a critical
period in development could alter the brain
growth trajectory in fish, but a follow-up study
on Atlantic salmon where brains were sampled
repeatedly over development showed that this
was probably not the case as effects on brain size
disappeared gradually after the fish was removed
from enriched environments (N
aslund et al.
2012). These studies on gross relative brain size
do, however, not provide direct evidence for
actual increase in brain cell numbers, as the
brain size effects may not be directly dependent
on neurogenesis. For instance, in the study of
Lema et al. (2005), higher proliferation rates of
cells in the forebrain were not translated into lar-
ger forebrain size. It should be pointed out that if
EE reduces the growth rate, EE-reared fish may
end up with larger relative brain size as a conse-
quence of altered growth allometry, as slow grow-
ers could have larger brains in relation to their
bodies, compared with fast-growing conspecifics
(Devlin et al. 2012). Furthermore, even if some
studies suggest that captive fish have smaller
brains than wild conspecifics (Marchetti and Ne-
vitt 2003; Burns et al. 2009; Mayer et al. 2011),
other studies on captive reared fish released into
natural, or semi-natural, environments show the
opposite effect (Kotrschal et al. 2012; N
et al. 2012). Although the latter results may seem
counterintuitive, brain growth is costly and may
be traded-off against somatic growth in food-lim-
ited natural environments, especially at early life
stages when mortality is high and strongly size-
Several studies indicate that EE could be effec-
tive in improving cognitive ability by enhancing
adaptability to novel situations and learning. In
Atlantic salmon, introducing temporally variable
structural EE had positive effects on both neuro-
genesis and learning ability in the context of
escaping a maze (Salvanes et al. 2013). In zebra-
fish, there are also some indications that wild
strains may have faster rate of learning if reared
in EE-tanks rather than the common barren envi-
ronments that are typically used (Spence et al.
2011). Lee and Berejikian (2008) found that rain-
bow trout reared in aquaria with stones and plas-
tic plants increased their exploratory behaviour
when the tank structures were stable, but not
when positions of structures varied in time, which
may have been an effect of frequent disturbance
distress. The trout reared in enriched aquaria also
showed less intraindividual behavioural variation,
whereas their feeding ability on novel drifting prey
was not improved. However, structural enrich-
ment effects on prey capture ability may also
require familiarity with novel prey (Sundstr
and Johnsson 2001). In a study on Atlantic
salmon, fish reared with EE foraged more effi-
ciently on novel prey, but only if they also had
experience of live food (Brown et al. 2003). Inter-
estingly, live food experience alone was not suffi-
cient to improve novel food foraging, so EE is
10 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
potentially important in this respect. Similarly,
several studies on Atlantic cod show that the pro-
vision of in-tank structures increases behavioural
flexibility and social learning (Braithwaite and
Salvanes 2005; Salvanes and Braithwaite 2005;
Strand et al. 2010).
Structures inducing environmental variability and
Environmental variability is often considered to
have stimulatory effects on learning and cognition
(e.g. Kuczaj et al. 2002; Watters 2009) and also
to affect the capacity for efficient resource defence
(Grant 1997). The rationale for introducing envi-
ronmental variation in the captive environment is
either that it will be stimulating because that is
what animals are adapted to in the wild, or that
uncertainty provides a (beneficial) psychological
challenge. For example, mammals and birds that
are given unpredictable access to EE objects inter-
act more with these objects than if their access is
predictable (Kuczaj et al. 2002). Temporal varia-
tion in structure positioning and food availability
has been found to alter behaviour, for example, by
reducing activity and reducing antipredator behav-
iour, in Atlantic cod (Salvanes and Braithwaite
2005, Braithwaite and Salvanes 2005). Atlantic
salmon reared under more nature-like and vari-
able conditions showed increased foraging ability
on natural prey and improved migration after
stocking, compared with barren-reared salmon
(Rodewald et al. 2011; Hyv
arinen and Rodewald
2013). However, effects of variation per se are
hard to infer, as few studies have compared stable
EE versus variable EE. In one study that did incor-
porate both stable and variable enrichment, rain-
bow trout from the stable EE were more
exploratory in a start-box emergence test than fish
from variable EE and also tended to be more
exploratory than fish from barren tanks (Lee and
Berejikian 2008). However, different species may
be differently affected by novelty, and effects are
also likely dependent on the frequency of distur-
bance. In a bird study, novel objects as EE were
considered negative as they increased stress levels
through neophobia (Fairhurst et al. 2011). Thus,
variation can potentially be negative in a func-
tions-based welfare concept, while it could be
regarded as positive in a nature-based concept if
variation stimulates adaptive behaviour through
novelty stress.
Tank floor substrates
Tank floor substrates could have several beneficial
effects for fish that interact with the bottom. It
may for instance reduce injuries in fish which nor-
mally rest at the bottom of the tanks, for example,
salmonid juveniles and pleuronectiforms (flatfish-
es). Consistently, rainbow and cutthroat trout
reared in raceways supplied with cobble showed
less fin damage than those reared without sub-
strate, which may be due to both reduced abrasion
with the environment and reduced aggression
(Bosakowski and Wagner 1995; Wagner et al.
1996; Arndt et al. 2001). In Atlantic halibut Hip-
poglossus hippoglossus (Pleuronectidae) juveniles,
rearing on smooth PVC increases external skin
lesions and limits the capacity for healing skin
damage, compared with rearing on substrates
such as sand, gravel or other artificial irregular
substrates (Ottesen and Strand 1996; Ottesen et al.
2007). In Dover sole Solea solea (Soleidae), sand
cures and eliminates outbreak of black patch
necrosis, probably due to the abrasive effect of
sand which remove pathogen-promoting dead cells
from the fish bodies (McVicar and White 1982;
McVicar 1987). Tank substrates may also provide
opportunity to learn burying behaviours in ben-
thic species like flatfishes (Ellis et al. 1997). This
could be beneficial if the fish are destined for
release as stock enhancement, but also within the
hatchery system if the fish are cannibalistic, like
for example juvenile olive flounder Paralichthys oli-
vaceus (Paralichthyidae) (Dou et al. 2000). Sand
substrates, which allows burying, also reduces res-
piration rate and resting metabolic rate in Dover
sole, indicating that sandy substrates provide less
stressful environments (Peyraud and Labat 1962;
Howell and Canario 1987). Substrates can also
eliminate the occurrence of ambicolouration (pig-
mented blind sides) in flatfishes (Rabben and Huse
1986; Kang and Kim 2012, 2013), which can
increase the appeal of cultured flatfish to custom-
ers in fish markets.
There may also be positive effects in species
which do not rest directly on the tank floor, but
interacts with benthos as part of their natural
behaviour. The absence of bottom substrate has,
for instance, been shown to increase the seroto-
nergic activity in crucian carp Carassius carassius
(Cyprinidae) held in aquaria for experimental pur-
poses (H
oglund et al. 2005). Addition of coloured
glass gravel as substrate in aquaria increased
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 11
Structural enrichment for captive fish JN
aslund and J I Johnsson
growth and reduced aggression and basal cortisol
levels while increasing the cortisol responsiveness
in gilthead seabream, which suggest lower stress
levels in the enriched environment (Batzina and
Karakatsouli 2012; Batzina et al. 2014a,c). Fur-
thermore, provision of sand in tanks for Mozam-
bique tilapia Oreochromis mossambicus (Cichlidae)
increased behavioural diversity in males, but not
in females, which probably has to do with repro-
ductive behaviours linked to the bottom substrates
(Galhardo et al. 2008).
It should be emphasized that usage of bottom
substrates may also lead to poor environmental
conditions and pathogen infections due to difficul-
ties in cleaning the substrates (Baynes and Howell
1993). Such effects were thought to be the reason
for the increased mortality rates of southern floun-
der Paralichthys lethostigma (Paralichthyidae)
reared with sand (Tuckey and Smith 2001).
Incubation substrates
Incubation substrates are added to mimic the nat-
ural environment for hatchlings, mainly with the
specific aim of producing fish more similar to nat-
ure-born fish for release into the wild (Bams and
Simpson 1977). Salmonid alevins (yolk-sac fry)
hatch from eggs buried in gravel and spend the
first time of their life within this substrate, and
thus, gravel was the first incubation substrate
tried out to improve the survival of alevins
released into the wild after hatching (Robertson
1919, Bams and Simpson 1977). However, the
bulky and heavy gravel requires hard work in
the hatcheries and, therefore, many studies have
evaluated replacement materials which are easier
to work with (Bailey and Taylor 1974). Some
alternative materials used are labyrinthine or
grooved plastic materials, grates, netting and
artificial turf mats. Substrates in general have
beneficial effects, but effects do differ among
types. For instance, substrates with greater void
space can lead to higher numbers of prematurely
emerging fry (Taylor 1984). See Table S2 for
details on effects from different incubation sub-
strate studies.
In general, adding incubation structures to
hatching troughs for salmonids have shown clear
beneficial effects during the alevin life stage and
alevins also prefer substrates over barren floor
when given a choice (Marr 1963; Benha
ım et al.
2009). The most typical effects are related to
growth and survival, which both are generally
improved by structure, with little difference among
different substrates (Taylor 1984; but see Br
1989). In the majority of studies on salmonids,
growth is improved during the alevin stage due to
better yolk utilization efficiency (see Table S2).
Only a few studies indicate slower (Bams 1983),
or equal (Nortvedt et al. 1985; Parker et al. 1990;
aslund et al. 2012) growth rates in substrates
compared with barren environments. Substrate-
induced growth effects are, however, not necessar-
ily maintained after the yolk-sac is consumed, as
some studies indicate compensation in growth rate
in post-alevin fry which were reared in barren
incubation troughs (Leon and Bonney 1979; Han-
sen and Møller 1985; Sveier and Raae 1992;
a 1993). There is consensus in the litera-
ture that the improved yolk utilization depends on
the lower swimming activity (lower ‘activity stress’
sensu Hansen and Møller 1985) of alevins reared
with structures (Marr 1963; Bams 1969; Hansen
et al. 1990; Peterson and Martin-Robichaud 1995;
ım et al. 2009).
Survival of alevins is improved by incubation
substrate in many studies (see Table S2). A few
studies show non-significant (Boyd 2001; Bamber-
ger 2009) or negative effects (Alan
a 1993).
Improved survival likely depends on reduced
occurrence of yolk-sac deformations. Lack of sub-
strate has been shown to be a principal cause of
yolk-sac constrictions and malformations, leading
to coagulated yolk in the distal parts of the sac
(Emadi 1972). Due to the high activity levels of
barren-reared alevins, the yolk-sac becomes more
elongated and thereby more easily constricted, and
the fish are more likely to abrade the sacs against
the floor, leading to rupture (Emadi 1972; Hansen
and Møller 1985). Alevins in barren troughs also
commonly position themselves in a vertical head-
down position, especially when reared in high
densities, which is likely innate escape behaviour,
where the fish swim downwards to bury in the
non-existing substrate (Emadi 1972; Murray and
Beacham 1986). This causes the oil-droplet in the
yolk-sac to be relocated, from the anterior or cen-
tral part of the sac to the posterior part, which
can lead to severe constriction and also deforma-
tion of internal organs (Emadi 1972). Damage to
the yolk-sac is likely to cause death, either imme-
diately or delayed (Emadi 1972). It should be
noted that not all species show increases in yolk-
sac deformations in barren environments, the
12 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
variation mainly depending on species differences
in alevin activity (see Emadi 1972). The density of
alevins also affects the frequency of sac constric-
tions, with more constrictions at higher densities,
which can eliminate the positive effects of sub-
strates on survival (Murray and Beacham 1986).
There may also be reductions in size-selective mor-
tality, where initially smaller fish with high yolk
reserves (and thus inferior swimming and feeding
ability) survive better in sheltered environments
(Hansen 1985).
Judging from the studies above, the main effects
of incubation substrate on salmonid alevins are
due to altered behaviour, mainly activity and
body-positioning behaviours. Particularly,
increased activity in barren troughs seems to stem
from the low static stability in alevins on plain
bottoms (Marr 1963; Emadi 1972; Blackett 1974;
Dill 1977; Benha
ım et al. 2009). The yolk-sac
makes alevins unstable; they easily roll over and
are consequently required to swim to maintain a
normal horizontal position (Marr 1963; Bams
1969; Gaignon and Prouzet 1982). Rugose sub-
strates permit the alevins to rest in a normal posi-
tion. Furthermore, disturbance in the hatchery
may contribute to the increased activity as well as
the head-down positioning. In contrast to static
stability problems, the disturbance may be reduced
by covering the troughs, or reducing light levels.
Structures in the alevin rearing environment
also affect the brain growth positively in salmonid
alevins (Kihslinger and Nevitt 2006; N
aslund et al.
2012). Kihslinger and Nevitt (2006) also observed
a reduced activity of the alevins in trays provided
with cobble. Enhanced brain growth could be due
to increased portion of energy available for neural
growth or, alternatively, due to increased stimula-
tion of sensory systems. An anecdotal observation
also indicates that Atlantic salmon alevins reared
in gravel substrate survived a period of unseason-
ably elevated water temperature substantially bet-
ter than barren-reared alevins (Bamberger 2009).
As an explanation, Bamberger (2009) hypothe-
sizes that the higher activity stress in the barren
environment could have led to more rapid oxygen
Whether or not the positive effects of incubation
substrates are translated into positive effects in
later stages of life is a question not widely
researched. As mentioned previously, size is often
compensated after the alevin stage in barren-
reared fish. Bams (1967) found improved swim-
ming ability and predator avoidance in gravel
reared fish, but still not as good as in wild fish.
Fuss and Johnson (1988) found improved raceway
survival in coho salmon parr in substrate reared
fish, but no effects on marine survival.
Incubation substrates have also been used for
species other than salmonids, but to a much lower
extent. In Atlantic sturgeon Acipenser oxyrinchus
(Acipenseridae) yolk-sac larvae, survival has been
shown to be negatively affected by substrate (Gess-
ner et al. 2009; Wiszniewski et al. 2010), while
growth has been either positive (Wiszniewski et al.
2010) or negative (Gessner et al. 2009). In white
sturgeon Acipenser transmontanus (Acipenseridae),
effects were similar to the ones observed for sal-
monids, with increased yolk absorption efficiency
and improved growth, condition and survival
(Boucher et al. 2014). In African sharptooth cat-
fish, the egg-hatching rate is improved by natural
plant substrates, but reduced by artificial mats
(Macharia et al. 1998). These effects were attrib-
uted to improved egg oxygenation in plant sub-
strates (Macharia et al. 1998). Finally, yolk-sac
larvae of Japanese eels Anguilla japonica (Anguilli-
dae) had greatly reduced survival in the presence
of sand or silt as bottom substrate (Chang et al.
Potentially negative effects of incubation sub-
strates include increased risk of fungal infections
due to food particles being trapped in the sub-
strates (Alan
a 1993). Some structures may also
harm the fish, like vinyl loop carpet with large
loops, in which the fish gets trapped and suffocates
(Gaignon and Prouzet 1982).
Toys are often added as enrichment in enclosures
for mammals (Newberry 1995; van Praag et al.
2000). The underlying motivation for usage of
toys is that there is a functional significance, that
is, a need for play (Hall 1998). Even if a few fish
species use objects in a manipulative way (Brown
2012), the relevance of toys for fish is unclear.
Play behaviour has been suggested to occur in
fish, but evidence remain anecdotal and controver-
sial (Burghardt 2005). Toys may be used as novel
objects in an unpredictable environment, but as
such there are also risks of neophobic reactions
leading to reduced welfare. Zimmermann et al.
(2012) used two kinds of ball toys as potential
stimulatory objects for Atlantic cod in net cages,
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 13
Structural enrichment for captive fish JN
aslund and J I Johnsson
but the fish did not interact much with these
Physical structures in combination with other
types of enrichment
Many studies have used non-factorial experimental
combinations of submerged structures along with
underwater feeders, tank covers, natural food, pre-
dation simulation and varying water current and
depth (Berejikian et al. 1999, 2000, 2001; Riley
et al. 2005, 2009; Berejikian and Tezak 2005;
Kihslinger et al. 2006; Gerasimov and Stolbunov
2007; Tatara et al. 2008, 2009; Fast et al. 2008;
Roberts et al. 2011; Rodewald et al. 2011; Hyv
nen and Rodewald 2013). Effects of the treatments
differ, probably due to enrichment type, species
and life stage differences. Some of the significant
effects obtained are increased dominance in
enriched fish compared with barren-reared conspe-
cifics (Berejikian et al. 2000, 2001), improved per-
formance (e.g. foraging or migration success) in
natural or semi-natural environments (Rodewald
et al. 2011; Hyv
arinen and Rodewald 2013) and
reduced fin damage (Berejikian and Tezak 2005).
However, interaction effects between different
environmental factors are likely, as seen in, for
example, pigs and vipers (Bonnet et al. 2013; Guy
et al. 2013). Due to the fact that many types of
environmental manipulations have been combined
in these studies, there is no possibility to pinpoint
which specific factors are influencing the fish, their
relative importance or their cost-efficiency. Still,
while there are possible risks that multiple simul-
taneous manipulations interact to cancel out posi-
tive effects, non-factorial studies using several
types of EE have nevertheless provided important
insights to the effects of enriching the captive envi-
ronment. Factorial experimental designs should,
however, be the next step in follow-up studies
aiming at optimizing EE strategies.
Structures in periphyton-based aquaculture
Addition of structures can be a way of increasing
the production in aquaculture systems, as it pro-
vides well-oxygenated surfaces for periphyton
(a matrix of bacteria, algae and other microorgan-
isms) to grow on, which in turn can be consumed
by the fish (van Dam et al. 2002; Bosma and Ver-
degem 2011). Applications of periphyton sub-
strates are widely researched within tropical
cyprinid and cichlid aquaculture (Fig. 1), with
considerable benefits for fish growth and survival
(van Dam et al. 2002; Azim et al. 2005). Many
structures used are locally produced organic mate-
rials such as bamboo or sugarcane fibrous matter
(e.g. Keshavanath et al. 2004; Uddin et al. 2007).
Artificial substrates, such as PVC pipes or plastic
slides, have also been used but periphyton tends to
grow better on natural substrates (van Dam et al.
2002). Survival and growth of the fish is positively
influenced in some, but not all, species (Azim et al.
2001; Sahu et al. 2007). Even though this appli-
cation of structures in aquaculture is not com-
monly described as a structural EE strategy, it
may likely affect the fish in similar ways and can
be considered as EE following the definition pre-
sented above. For instance, addition of periphyton
structures can lead to improved functional welfare
by increased immunity towards Aeromonas hydro-
phila in rohu carp Labeo rohita (Cyprinidae) (Rajesh
et al. 2008). Whether there are also benefits to
feelings-based welfare remains to be investigated.
As this kind of enrichment has been reviewed
thoroughly (van Dam et al. 2002, Azim et al.
2005), we do not delve deeper into the effects
here. However, a bibliography of papers investigat-
ing effects of periphyton substrates on fish, on
which Fig. 1 is based on, is presented in Table S3
(electronic supplement).
Treatments closely related to structural
Tank cover
The environment outside an enclosure may also
influence captive animals, an effect described as
the ‘room with a view-effect’ in zoo management
(Newberry 1995). However, in contrast to zoo
keeping, the aim in fish rearing has traditionally
not been to increase the stimulation from the
external environment, but rather to limit it to
reduce the amount of potential stressors affecting
the fish, for example, by adding covers on top of
the tanks. As the aim then is to reduce informa-
tion transmitted from outside, full cover of tanks
should perhaps not be considered as EE. It may
nevertheless be beneficial from a function- or feel-
ings-based welfare approach, as it can reduce
stressful stimuli (Allen 1973; Roadhouse et al.
1986). It may also provide preferred lighting con-
ditions for nocturnal species like African sharp-
14 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
tooth catfish (Hossain et al. 1998, Britz and Pie-
naar 1992). In contrast, partial cover could poten-
tially be regarded as EE as it adds environmental
complexity in the form a gradient of light inten-
sity. Particularly, partial cover provides the fish
with a choice of sheltering from the external world
underneath the cover, which is a natural behav-
iour in many fish species (e.g. Nordgreen et al.
2013). Some effects from tank covers may thus be
the same as effects seen from supplying in-tank
shelters. If so, tank cover could be a better option
because it is a cheaper EE strategy than in-tank
structures, as it requires less maintenance. How-
ever, some effects of in-tank shelters cannot be
obtained by using cover lids, for example, visual
barriers between fish in the tank and shelter from
aggressive individuals.
Several studies on salmonids show that partial
covers are utilized by the fish (e.g. Wagner et al.
1995; Barnes et al. 2005; Smith 2011, Nordgreen
et al. 2013). However, even within the salmonid
group, there are considerable species differences in
preference and not all species prefer cover (Butler
and Hawthorne 1968; Heggenes and Traaen
1988). There are also differences in preference
depending on temperature (Heggenes and Traaen
1988), age (Kwain and MacCrimmon 1969) and
size of cover (Butler and Hawthorne 1968). In gen-
eral, effects on growth and survival also differ lar-
gely among species. For instance, Atlantic salmon
were less stressed and grew better with partial
cover, while no effects were seen on brown or rain-
bow trout (Pickering et al. 1987). Northern pike
Esox lucius (Esocidae) grew better with cover but
also survived less well due to increased cannibalism
and natural mortality (Szczepkowski 2009). Coho
salmon survived better in covered than in uncov-
ered raceways (Fuss and Johnson 1988), while no
significant effects were seen in rainbow trout or
brown trout Salmo trutta (Salmonidae) reared in
hatchery tanks (Barnes and Durben 2003; Barnes
et al. 2005). In pond-reared channel catfish Ictalu-
rus punctatus (Ictaluridae), floating covers had over-
all negative effects on both growth and survival
(Phelps and Silva De Gomez 1992). Overall, effects
of partial tank cover are variable, largely depending
on species ecology and how the cover is applied.
Pond rearing
Pond rearing is an old aquaculture technique but
remains as the major rearing environment for fish
in the world (FAO 2014). Pond rearing often
incorporates some aspect of structural EE, as well
as some potentially enriching factors, such as nat-
ural variability, live prey and sometimes predation.
Ponds can also be additionally enriched by addi-
tion of structures (e.g. Herbert et al. 2003).
Experiments on pikeperch Sander lucioperca (Per-
cidae) have shown that juveniles reared in ponds
differ in their habitat choice as compared to hatch-
ery-reared fish. Pond fish use vegetation to a
higher extent than hatchery-reared fish and also
change habitat more frequently. The pond-reared
pikeperch also had more active antipredator
behaviour and better foraging ability on novel live
prey. The size of the fish, however, was smaller
than in the hatchery (Ahlbeck and Holliland
2012). Pond rearing, as compared to tank rearing,
had positive effects on recapture rates of European
grayling Thymallus thymallus (Salmonidae) and
brown trout stocked into natural rivers (N
1992; Turek et al. 2012). However, other studies
on the same species have shown negligible or con-
trasting effects (Johnsen and Hesthagen 1990;
Turek et al. 2010). Rainbow trout reared in ponds
with added structures during the last months pre-
ceding smoltification had enhanced physiological
smolt characteristics, as compared to fish kept in
concrete raceways (Zydlewski et al. 2003) and
marine survival of the same species have been
improved by pond rearing as compared to rearing
in raceways (Tipping 1998). As a non-salmonid
example, June suckers Chasmistes liorus (Catostom-
idae) reared in reservoirs prior to release had bet-
ter post-release performance than hatchery-reared
individuals in one case, but not in another (Ras-
mussen et al. 2009).
Positive effects may be due to naturalization,
where the fish adapts to a life in the wild. How-
ever, as some studies show negligible or negative
effects, there are probably other factors which
need to be considered as well. The nature of the
pond and the time spent there has for instance sig-
nificant influence on the marine survival of salmo-
nids. Earthen-bottom ponds produced rainbow
trout with higher marine survival than asphalt-
bottom ponds (Tipping 2008), and longer time in
the pond prior to release increased marine survival
of cutthroat trout (Tipping 2001).
Wild-reared fish often perform better in the wild
than pond-reared fish (Miller 1954; Turek et al.
2012), suggesting that even if pond rearing
increases the natural fitness of fish compared with
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 15
Structural enrichment for captive fish JN
aslund and J I Johnsson
tank-rearing, it is still not alleviating all maladap-
tive effects of artificial rearing. There are also some
other potential problems associated with pond
rearing, like high temperatures, harvest ineffi-
ciency and distasteful flavour of the fish (Lawler
et al. 1974).
Potential problems with environmental
Application of EE can be associated with some
problems, compared with sterile barren environ-
ments (Hare et al. 2008; Williams et al. 2009).
Accordingly, aquaculture managers are often con-
cerned about application of enrichments. For
instance, accumulation of food particles and faeces
in enriched tanks are common concerns (e.g. Bay-
nes and Howell 1993). Therefore, tank cleaning
should be taken into account when EE is consid-
ered (e.g. efforts of manual labour or application
of bottom filters). Bottom filters can be utilized in
some cases where loose substrates are used, as is
common in ornamental aquaria. Structural
enrichment may also be vectors for pathogens
(Tuckey and Smith 2001; J. I. Johnsson personal
observation). In addition, enrichment structures
could also leak potentially hazardous chemicals
(e.g. phtalates leaking from PVC, Clark et al.
Problems may also arise from application of
unsuitable enrichment which disturb, injure or
stress the fish and thus creates a low-welfare envi-
ronment resulting in harm or death to the fish.
Structural enrichment creating loops, holes and
crevices may for instance lead to body entrapment
and suffocation (see e.g. Gaignon and Prouzet
1982; Nguyen and Crocker 2007). Addition or
alteration of structures may also lead to distress
due to e.g. neophobia (Fairhurst et al. 2011). Shel-
ters may lead to reduced feeding and growth, and
possibly to low oxygen levels if high numbers of
fish shelter together. Addition of too few EE struc-
tures may also cause problems, as a few defend-
able structures can increase aggression (Gwak
2003; Mikheev et al. 2005; Barreto et al. 2011).
Post-release effects: do enriched sh perform
Being released into an unfamiliar environment is
probably a tough experience for most animals.
Even if many species show considerable pheno-
typic plasticity, the speed of acclimation and the
range of environments to which acclimation is
possible, are limited by genetic and developmental
constraints (Pigliucci 2001). For instance, translo-
cated birds show resting disorders which could
lead to cognitive impairments and low post-release
survival (Henry et al. 2013). The same may be
true in fishes, as brown trout which were accli-
mated before release (so-called ‘soft release’) sur-
vived better than fish released directly into their
new home environment (Jonsson et al. 1999;
Brennan et al. 2006; Strand and Finstad 2007).
The more different the novel environment is from
the previously experienced environment, the stron-
ger the stress response may be and/or the longer
it may take to learn to behave adaptively in the
new environment but direct investigations of
this hypothesis are lacking. Much of the post-
release mortality appears to occur shortly after
release (e.g. McCrimmon 1954; Brockmark et al.
2010); indicating that adaptive traits during this
initial period in the wild should be targeted. Sev-
eral studies show that EE-reared rainbow trout
increase their competitive ability in semi-natural
environments (Berejikian et al. 2000, 2001; Tat-
ara et al. 2008). Moreover, Atlantic salmon juve-
niles reared with EE are more efficient foragers in
the wild (Rodewald et al. 2011). White seabream
conditioned with shelters and/or predator experi-
ence had substantially higher estimated sea sur-
vival than unconditioned white seabream (D’Anna
et al. 2012). In the same study, shelter condi-
tioned seabream also dispersed less from the
release point. Another study on Atlantic salmon
indicates that the survival of migrating smolts can
be improved by rearing in enriched environment
arinen and Rodewald 2013). The latter study
incorporated several enriching features, for exam-
ple, structures and water current variability, and
it is not possible to isolate which factor(s) that led
to the positive effects. Several studies investigating
post-release effects have not been able to detect
any positive effects from EE when compared to
barren rearing (Berejikian et al. 1999; Brockmark
et al. 2007, 2010; Tatara et al. 2008, 2009; Fast
et al. 2008). Some effects of enrichment may be
counteracted by other treatments in the hatchery.
For instance, starvation before release may
increase activity and risk taking irrespective of
prior rearing environment (Moberg et al. 2011).
Fish may also forage suboptimally just after
release, as shown in meagre Argyrosomus regius
16 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
(Sciaenidae) (Gil et al. 2014), which could
enhance the impact of negative experiences just
prior to release. Therefore, care must be taken to
provide as good release conditions as possible.
To summarize the effects of EE on post-release
performance: only few studies have tested post-
release effects in fish and results are mixed, even
among closely related species. There are critical
needs for further research in this area, to make it
possible to assess whether there are any general
benefits in usage of EE in stock-fish hatcheries.
Preferences: what do the shes actually want?
Preference tests could be used to gain knowledge
about which environment an animal desire (Daw-
kins 2006; Volpato et al. 2007). A number of
studies indicate that fish have innate preferences
for certain environments, which then can be used
for designing appropriate EE. For instance, in juve-
nile lake sturgeon Acipenser fulvescens (Acipenseri-
dae), the habitat preference for plain sandy
bottoms is not altered by hatchery rearing in bar-
ren tanks (Peake 1999). This is also the case in
hatchery-reared flatfishes, which have similar pref-
erences for sandy or muddy substrates as their
wild conspecifics (Ellis et al. 1997; Tuckey and
Smith 2001), and long-snouted seahorses Hippo-
campus guttulatus (Syngnathidae), where aquar-
ium-reared individuals have similar preferences for
structures to use as holdfasts, as wild conspecifics
(Faleiro et al. 2008). Many captive species do
indeed show preferences for structural enrichment
when given a choice, at least in some contexts.
Salmonid alevins (yolk-sac fry) show preference for
structured substrate in hatcheries (Marr 1963; Be-
ım et al. 2009) and several cichlid species pre-
fer structured environments over barren, at least
in association with reproduction (Delicio et al.
2006; Galhardo et al. 2009; Freitas and Volpato
2013). Several common ornamental aquarium,
and laboratory, species seem to prefer to associate
with tank enrichments such as plants, but group
size, sex and species composition in the aquarium
will also influence the habitat choice (Delaney
et al. 2002; Saxby et al. 2010; Kistler et al. 2011;
Sloman et al. 2011; Schroeder et al. 2014).
Specific preferences differ among species, but
also among populations and age classes. White
sturgeons prefer to hide under rocks the first two
weeks after hatching, whereupon they switch to
using open habitats (Kynard et al. 2013). Simi-
larly, gilthead seabream appear to have age-depen-
dent preferences for gravel colour (Batzina et al.
2014d). Studies on wild and hatchery red drum
Sciaenops ocellatus (Sciaenidae) and cutthroat trout
in semi-natural environments showed that hatch-
ery fish of both species were less specific in their
habitat choice than wild conspecifics (Mesa 1991;
Stunz et al. 2001). Such habitat preferences are
often time-dependent. For example, pond-reared
rainbow trout diverged from laboratory-reared
trout in their preference for tank background col-
our over time (Ritter and MacCrimmon 1973).
These latter examples indicate that hatchery selec-
tion and/or habituation can alter the preference,
and thus, preference tests may not always work
for selecting enrichments for nature-based welfare
aims. However, it does show what the fish prefer,
which is appropriate from a feelings-based perspec-
tive (Volpato et al. 2007).
Importantly, some other species do not always
prefer structural enrichment. Beluga sturgeon
Huso huso (Acipeseridae) juveniles generally prefer
smooth bottoms, for example, concrete, over
gravel (Falahatkar and Shakoorian 2011). This
may be an effect of an overall preference for plain
sandy substrates, a bottom type which was not
present in the study, but shown to be strongly pre-
ferred by another sturgeon species (Peake 1999).
Thus, in some cases, it may be better to keep the
hatchery environment simple rather than provid-
ing the wrong kind of EE. Sometimes the fish pre-
fer certain types of EE over other, even though
they seem to have the same function from a
human perspective. This is exemplified by the
higher utilization of clay brick shelters compared
to PVC pipes in zebra plecos Hypancistrus zebra
(Loricariidae) (Ramos et al. 2013).
Finally, to assess how important one type of EE
is to the fish, it can be valuable to investigate how
strong the preferences are. Mozambique tilapia, for
instance, work harder for food and social company
than for additional space (Galhardo et al. 2011).
Eurasian perch juveniles associate with tank struc-
tures and also appear to compete for them, leading
to high aggression levels when shelters are limited
(Mikheev et al. 2005).
General considerations for environmental
enrichment research in sh
Shepherdson (2003) listed four steps for a success-
ful EE strategy: (i) compare wild and captive
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 17
Structural enrichment for captive fish JN
aslund and J I Johnsson
environments and behaviours, (ii) set goals for the
desired effect, (iii) design and implement the EE,
and (iv) assess and evaluate the strategy.
First of all, knowledge of the biology of the tar-
get species is of profound importance when apply-
ing EE (Olsson and Dahlborn 2002). Not all
successful enrichment strategies are based on nat-
ural environments or stimuli, but natural behav-
iours and environments can give important hints
to what may produce the desired effects (Mellen
and Sevenich MacPhee 2001; Wells 2009). The
species biology may also vary over different life
stages or for different populations (e.g. Manosevitz
and Montemayor 1972; Gonda et al. 2009).
Importantly, the biology of a domesticated species
may differ substantially from the wild conspecifics
(e.g. Gross 1998), thus, mimicking the wild is not
necessarily the optimal strategy in all cases (Vea-
sey et al. 1996; Shepherdson et al. 1998). Prefer-
ence tests, followed by studies investigating the
strength of the preferences can be used to assess
the importance of EE (Olsson and Dahlborn 2002).
It should also be clear that even an enriched cap-
tive environment is still deprived compared with
natural habitats, and goals should be adapted to
this fact (Burghardt 1999). Furthermore, some
kinds of enrichments may not give the desired
effects, and some could even be deleterious (Hare
et al. 2008). Before applying enrichment in a large
scale, the effects should be evaluated to avoid det-
rimental effects and unnecessary costs and labour.
To be able to sort out specific effects, particu-
larly interactions, of different types of enrichment,
studies should be based on factorial designs when
possible. This may not be feasible if many enrich-
ment types are investigated simultaneously. In
cases where the number of tanks required for com-
plete replication of the design outgrows the
resources available, fractional factorial designs
may be a choice. Fractional designs can be used to
screen many factor combinations for effects in
experiments (see e.g. Trabelsi et al. 2011) and
could be beneficial in EE research as well.
If the fish is destined to be released into the
wild, assessment of its post-release performance
should preferentially be conducted. Relatively few
studies have been made to assess how stocking
effectiveness is affected by EE. More such investiga-
tions are warranted, especially as those conducted
so far show mixed effects (see section: Post-release
effects). It is possible that stress at release may
reduce effects of EE, so it could also be combined
with different release strategies such as night-time
release or pre-release acclimatization (see e.g. Jons-
son et al. 1999; Brennan et al. 2006; Strand and
Finstad 2007; Roberts et al. 2009); investigations
are needed in this area as well.
Some EE techniques presented here are not
extensively studied. For instance, information is
lacking on effects of variable EE as compared to
stable EE. Moreover, investigations of different
amounts of enrichment and interaction effects
with other environmental factors such as tank
density should be further investigated. Other inter-
esting areas of research concern the effects of
structures for periphyton-based aquaculture and
whether these have additional welfare benefits.
Many fish taxa are understudied with respect to
EE. For instance, studies on elasmobranchs are prac-
tically absent in the current literature (but see Smith
2006 for an EE plan). Furthermore, with respect to
the multitude of species present in the ornamental
fish trade, surprisingly few species have been sys-
tematically investigated with respect to their perfor-
mance in different environments (but see Kistler
et al. 2011). However, much information, albeit lar-
gely anecdotal, is found in the aquarist literature.
Surprisingly, despite the potential importance of
structural EE for the behaviour and physiology of
fishes, our survey of studies made on captive fish,
show that few researchers appear to utilize EE in
their experimental tanks (Fig. 2). Several of the
surveyed studies, do not mention whether or not
EE has been applied, which can be problematic for
replication of the studies. Due to the variable
effects of different kinds of EE, detailed information
on structures in the tank environment is vital for
interpreting results.
Concluding remarks
The understanding of how EE affects captive fish is
gradually increasing, with a substantial amont of
scientific papers published at this time. Many stud-
ies suggest that there are indeed effects of EE on,
for example, behaviour, growth performance, sur-
vival and physiology. Some, but importantly not
all, effects are positive from the perspective of the
culturist. There is also still much ambiguity with
respect to the consistency of the effects, both
among and within species. For these reasons, it is
important to continue to investigate the effects of
EE. More focus needs to be put on factorial
designs, investigating the specific effects of different
18 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
environmental alterations and their interactions.
More details are also needed on the effects on dif-
ferent life stages within single species. Further-
more, it is advisable to use several levels of
enrichment to be able to optimize the amount of
structures or substrate needed for reaching the
effects wanted. Cost-benefit analyses are needed to
investigate the economical aspects of the usage of
EE. However, the ethical perspective with respect
to fish welfare, both in captivity and in the wild
following stocking, needs to be incorporated in
such analyses. Finally, given the multitude of pos-
sible effects of EE, we suggest that future reports
from studies on captive fish should explicitly state
whether or not EE was used.
We thank Fredrik Nordwall, Staffan Andersson
and two anonymous reviewers for constructive
and thoughtful comments on the manuscript. This
study was conducted as part of the strategic pro-
ject SMOLTPRO, financed by the Swedish Research
Council Formas.
Ahlbeck, I. and Holliland, P.B. (2012) Rearing environ-
ment affect important life skills in pikeperch (Sander lu-
cioperca). Boreal Environment Research 17, 291304.
a, A. (1993) Significance of substrate and the tim-
ing of start-feeding in alevins of Arctic charr (Salvelinus
alpinus). Aquaculture 116,4755.
Allen, K.O. (1973) Effect of overhead cover on growth
and survival of channel catfish in circular tanks. The
Progressive Fish-Culturist 35, 213.
Allen-Ankins, S., Stoffels, R.J., Pridmore, P.A. and Vogel,
M.T. (2012) The effects of turbidity, prey density and
environmental complexity on the feeding of juvenile
Murray cod Maccullochella peelii.Journal of Fish Biology
80, 195206.
Allouche, S. (2002) Nature and functions of cover for
riverine fish. Bulletin Franc
ßais de la P^
eche et de la Pisci-
culture 365/366, 297324.
Anders, P.J. (1998) Conservation aquaculture and
endangered species. Fisheries 23,2831.
Angermeier, P.L. and Karr, J.R. (1984) Relationships
between woody debris and fish habitat in a small
warmwater stream. Transactions of the American Fisher-
ies Society 113, 716726.
Araki, H., Berejikian, B.A., Ford, M.J. and Blouin, M.S.
(2008) Fitness of hatchery-reared salmonids in the
wild. Evolutionary Applications 1, 342355.
Arndt, R.E., Routledge, M.D., Wagner, E.J. and Mellen-
thin, R.F. (2001) Influence of raceway substrate and
design on fin erosion and hatchery performance of
rainbow trout. North American Journal of Aquaculture
63, 312320.
Azim, M.E., Wahab, M.A., van Dam, A.A., Beveridge,
M.C.M. and Verdegem, M.C.J. (2001) The potential
of periphyton-based culture of two Indian major
carps, rohu Labeo rohita (Hamilton) and gonia
Labeo gonius (Linnaeus). Aquaculture Research 32, 209
Azim, M.E., Verdegem, M.C.J., van Dam, A.A. and Beve-
ridge, M.C.M. (2005) Periphyton: ecology, exploitation
and management. CABI Publishing, Wallingford.
Bailey, J.E. and Taylor, S.G. (1974) Plastic turf substitute
for gravel in salmon incubators. Marine Fisheries
Review 36,3538.
Bamberger, A. (2009) Semi-natural incubation tech-
niques for Atlantic salmon, Salmo salar: opportunities
and limitations for restocking. Aquaculture 293, 221
Bams, R.A. (1967) Differences in performance of natu-
rally and artificially propagated sockeye salmon
migrant fry, as measured with swimming and preda-
tion tests. Journal of the Fisheries Research Board of Can-
ada 24, 11171153.
Bams, R.A. (1969) Adaptations of sockeye associated
with incubation in stream gravel. In: Symposium on
salmon and trout in streams. H. R. MacMillan Lectures in
Fisheries. (ed. T.G. Northcote). University of British
Columbia, Vancouver, pp. 7188.
Bams, R.A. (1983) Early growth and quality of chum
salmon (Oncorhynchus keta) produced in keeper chan-
nels and gravel incubators. Canadian Journal of Fisheries
and Aquatic Sciences 40, 499505.
Bams, R.A. and Simpson, K. (1977) Substrate incubators
workshop - 1976. Report on current state-of-the-art. Fish-
eries and Marine Service, Nanaimo. 68 pp.
Baras, E., Tissier, F., Philippart, J.-C. and M
elard, C.
(1999) Sibling cannibalism among juvenile vundu
under controlled conditions. II. Effect of body weight
and environmental variables on the periodicity and
intensity of type II cannibalism. Journal of Fish Biology
54, 106118.
Barcellos, L.J.G., Kreutz, L.C., Quevedo, R.M. et al. (2009)
Influence of color background and shelter availability
on jundi
a(Rhamdia quelen) stress response. Aquaculture
Barley, A.J. and Coleman, R.M. (2010) Habitat structure
directly affects aggression in convict cichlids Archocen-
trus nigrofasciatus.Current Zoology 56,5256.
Barnes, M.E. and Durben, D.J. (2003) Effects of partial
tank covers on the growth of juvenile feral rainbow
trout during hatchery rearing. North American Journal
of Aquaculture 65, 344348.
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 19
Structural enrichment for captive fish JN
aslund and J I Johnsson
Barnes, M.E., Miller, J. and Durben, D.J. (2005) Partial
overhead tank cover use during feral brown trout rear-
ing. North American Journal of Aquaculture 67, 319
Barreto, R.E., Carvalho, G.G.A. and Volpato, G.L. (2011)
The aggressive behavior of Nile tilapia introduced into
novel environments with variation in enrichment.
Zoology 114,5357.
Basquill, S.P. and Grant, J.W.A. (1998) An increase in
habitat complexity reduces aggression and monopoliza-
tion of food by zebra fish (Danio rerio). Canadian Journal
of Zoology 76, 770772.
Batzina, A. and Karakatsouli, N. (2012) The presence of
substrate as a means of environmental enrichment in
intensively reared gilthead seabream Sparus aurata:
growth and behavioral effects. Aquaculture,370371,
Batzina, A., Dalla, C., Papadopoulou-Daifoti, Z. and Ka-
rakatsouli, N. (2014a) Effects of environmental enrich-
ment on growth, aggressive behaviour and brain
monoamines of gilthead seabream Sparus aurata reared
under different social conditions. Comparative Biochem-
istry and Physiology Part A: Molecular & Integrative
Physiology 169,2532.
Batzina, A., Dalla, D., Tsopelakos, A., Papadoupolou-Daif-
oti, Z. and Karakatsouli, N. (2014b) Environmental
enrichment induces changes in brain monoamine lev-
els in gilthead seabream Sparus aurata.Physiology &
Behavior 130,8590.
Batzina, A., Kalogiannis, D., Dalla, C., Papadopoulou-
Daifoti, Z., Chadio, S. and Karakatsouli, N. (2014c)
Blue substrate modifies the time course of stress
response in gilthead seabream Sparus aurata.Aquacul-
ture 420421, 247253.
Batzina, A., Sotirakoglou, K. and Karakatsouli, N.
(2014d) The preference of 0+and 2+gilthead
seabream Sparus aurata for coloured substrates or no-
substrate. Applied Animal Behaviour Science 151, 110
Baynes, S.M. and Howell, B.R. (1993) Observations on
the growth, survival and disease resistance of juvenile
common sole, Solea solea (L.), fed Mytilus edulis L.
Aquaculture and Fisheries Management 24,95100.
Benefiel, A.C., Dong, W.K. and Greenough, W.T. (2005)
Mandatory “enriched” housing of laboratory animals:
the need for evidence-based evaluation. ILAR Journal
ım, D., Leblanc, C.A. and Lucas, G. (2009) Impact
of a new artificial shelter on Arctic charr (Salvelinus al-
pinus, L.) behaviour and culture performance during
the endogenous feeding period. Aquaculture 295,
Berejikian, B.A. and Tezak, E.P. (2005) Rearing in
enriched hatchery tanks improves dorsal fin quality of
juvenile steelhead. North American Journal of Aquacul-
ture 67, 289293.
Berejikian, B.A., Smith, R.J.F., Tezak, E.P., Schroder, S.L.
and Knudsen, C.M. (1999) Chemical alarm signals and
complex hatchery rearing habitats affect antipredator
behavior and survival of chinook salmon (Oncorhyn-
chus tshawytscha) juveniles. Canadian Journal of Fisheries
and Aquatic Sciences 56, 830838.
Berejikian, B.A., Tezak, E.P., Flagg, T.A., LaRae, A.L.,
Kummerow, E. and Mahnken, C.V.W. (2000) Social
dominance, growth, and habitat use of age-0 steelhead
(Oncorhynchus mykiss) grown in enriched and conven-
tional hatchery rearing environments. Canadian Journal
of Fisheries and Aquatic Sciences 57, 628636.
Berejikian, B.A., Tezak, E.P., Riley, S.C. and LaRae, A.L.
(2001) Competitive ability and social behaviour of
juvenile steelhead reared in enriched and conventional
hatchery tanks and a stream environment. Journal of
Fish Biology 59, 16001613.
Bergman, E., Piccolo, J. and Greenberg, L. (2013) Raising
brown trout (Salmo trutta) with less food effects on
smolt development and fin damage. Aquaculture
Research 44, 10021006.
Bergqvist, J. and Gunnarsson, S. (2011) Finfish aquacul-
ture: animal welfare, the environment, and ethical
implications. Journal of Agricultural and Environmental
Ethics 26,7599.
Blackett, R.F. (1974) Preliminary evaluation of pink (On-
corhynchus gorbuscha) and sockeye (O. nerka) salmon
incubation and rearing in gravel incubators and troughs.
Alaska Department of Fish & Game, Juneau. 37 pp.
Blaxter, J.H.S. (1970) Sensory deprivation and sensory
input in rearing experiments. Helgol
ander wissenschaftli-
che Meeresuntersuchungen 20, 642654.
Bonnet, X., Fizesan, A. and Michel, C.L. (2013) Shelter
availability, stress level and digestive performance in
the aspic viper. The Journal of Experimental Biology
216, 815822.
Bosakowski, T. and Wagner, E.J. (1995) Experimental
use of cobble substrates in concrete raceways for
improving fin condition of cutthroat (Oncorhynchus
clarki) and rainbow trout (O. mykiss). Aquaculture 130,
Bosma, R.H. and Verdegem, M.C.J. (2011) Sustainable
aquaculture in ponds: principles, practices and limits.
Livestock Science 139,5868.
Boucher, M.A., McAdam, S.O. and Shrimpton, J.M.
(2014) The effect of temperature and substarte on the
growth, development and survival of larval white stur-
geon. Aquaculture 430, 139148.
Bovenkerk, B. and Meijboom, F.L.B. (2012) Fish welfare
in aquaculture: explicating the chain of interactions
between science and ethics. Journal of Agricultural and
Environmental Ethics 26,4161.
Boyd, S.R. (2001) An evaluation of treatments to reduce
mortality from coagulated yolk disease in hatchery-
produced chinook salmon. North American Journal of
Aquaculture 63, 246251.
20 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
Braithwaite, V. (2010) Do fish feel pain? Oxford University
Press, Oxford.
Braithwaite, V.A. (2014) Pain perception. In: The Physi-
ology of Fishes. (eds D.H. Evans, J.B. Claiborne and S.
Currie), 4th edn. CRC Press, Boca Raton, pp.
Braithwaite, V.A. and Salvanes, A.G.V. (2005) Environ-
mental variability in the early rearing environment
generates behaviourally flexible cod: implications for
rehabilitating wild populations. Proceedings of the Royal
Society B 272, 11071113.
Brennan, N.P., Darcy, M.C. and Leber, K.M. (2006) Pred-
ator-free enclosures improve post-release survival of
stocked common snook. Journal of Experimental Marine
Biology and Ecology 335, 302311.
Britz, P.J. and Pienaar, A.G. (1992) Laboratory experi-
ments on the effect of light and cover on the behav-
iour and growth of African catfish, Clarias gariepinus
(Pisces: Clariidae). Journal of Zoology 227,4362.
Brockmark, S., Adriaenssens, B. and Johnsson, J.I.
(2010) Less is more: density influences the develop-
ment of behavioural life skills in trout. Proceedings of
the Royal Society B 277, 30353043.
Brockmark, S., Nereg
ard, L., Bohlin, T., Bj
ornsson, B.T.
and Johnsson, J.I. (2007) Effects of rearing density and
structural complexity on the pre- and postrelease per-
formance of Atlantic salmon. Transactions of the Ameri-
can Fisheries Society 136, 14531462.
Broom, D.M. (1998) Welfare, stress, and the evolution of
feelings. Advances in the Study of Behavior 27, 371
Brown, C. (2012) Tool use in fishes. Fish and Fisheries
13, 105115.
Brown, C. and Laland, K. (2001) Social learning and life
skills training for hatchery reared fish. Journal of Fish
Biology 59, 471493.
Brown, B.E., Inman, I. and Jearld, A. (1970) Schooling
and shelter seeking tendencies in fingerling channel
catfish. Transactions of the American Fisheries Society
99, 540545.
Brown, C., Davidson, T. and Laland, K. (2003) Environ-
mental enrichment and prior experience of live prey
improve foraging behaviour in hatchery-reared Atlan-
tic salmon. Journal of Fish Biology 63, 187196.
as, E. (1989) The use of a simulated redd for incu-
bating Baltic salmon (Salmo salar) and trout (Salmo tru-
tta) alevins. Aquaculture 83, 261267.
Burghardt, G.M. (1999) Deprivation and enrichment in
laboratory animal environments. Journal of Applied Ani-
mal Welfare Science 2, 263266.
Burghardt, G.M. (2005) The origins of vertebrate play:
fish that leap, juggle, and tease. In: The Genesis of
Animal Play. (ed G.M. Burghardt). MIT Press, Cam-
bridge, pp. 309358.
Burns, J.G., Saravanan, A. and Rodd, F.H. (2009) Rear-
ing environment affects the brain size of guppies:
lab-reared guppies have smaller brains than wild-
caught guppies. Ethology 115, 122133.
Butler, R.L. and Hawthorne, V.M. (1968) The reactions
of dominant trout to changes in overhead artificial
cover. Transactions of the American Fisheries Society 97,
Candolin, U. and Voigt, H.-R. (1998) Predator-induced
nest site preference: safe nests allow courtship in stick-
lebacks. Animal Behaviour 56, 12051211.
Carfagnini, A.G., Rodd, F.H., Jeffers, K.B. and Bruce,
A.E.E. (2009) The effects of habitat complexity on
aggression and fecundity in zebrafish (Danio rerio).
Environmental Biology of Fishes 86, 403409.
Carrigan, M. and Attalla, A. (2001) The myth of the
ethical consumer do ethics matter in purchase
behaviour? Journal of Consumer Marketing 18, 560
CCAC Canadian Council on Animal Care (2005) CCAC
guidelines on: the care and use of fish in research, teaching
and testing. Canadian Council on Animal Care, Ottawa.
Available on:
Chang, S.-L., Kou, G.-H. and Liao, I.C. (2003) Salinity
adaptation and subsidence attributes in the early
stages of Japanese eel (Anguilla japonica). Acta Zoologica
Taiwanica 14,3344.
Chittenden, C.M., Biagi, C.A., Davidsen, J.G., et al.
(2010) Genetic versus rearing-environment effects on
phenotype: hatchery and natural rearing effects on
hatchery- and wild-born coho salmon. PLoS ONE 5,
Christie, M.R., Marine, M.L., French, R.A. and Blouin,
M.S. (2012) Genetic adaptation to captivity can occur
in a single generation. Proceedings of the National Acad-
emy of Sciences of the United States of America 109,
CHSRG - California Hatchery Scientific Review Group
(2012) California Hatchery Review Report. US Fish and
Wildlife Service and Pacific States Marine Fisheries
Commission, online publication, 100 pp. Available at:
Clark, K., Cousins, I., MacKay, D. and Yamada, K.
(2003) Observed concentrations in the environment.
In: The Handbook of Environmental Chemistry, Vol 3,
Part Q: Phthalate Esters. (ed C.A. Staples). Springer-Ver-
lag, New York, pp. 125177.
Conrad, J.L., Weinersmith, K.L., Brodin, T., Saltz, J.B. and
Sih, A. (2011) Behavioural syndromes in fishes: a
review with implications for ecology and fisheries man-
agement. Journal of Fish Biology 78, 395435.
Costa, B.N., Kato, C.E., Andr
e, F.L., et al. (2011) Trying
out enrichment for red-bellied piranhas. The Shape of
Enrichment 20,45.
Coulibaly, A., Kon
e, T., Ouattara, N.I. et al. (2007)
uation de l’effet d’un syst
eme de refuge sur la survie et
la croissance des alevins de Heterobranchus longifilis
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 21
Structural enrichment for captive fish JN
aslund and J I Johnsson
es en cage flottante. Belgian Journal of Zoology 137,
157164. [In French.]
Council of Europe (2006) Appendix A of the European Con-
vention for the Protection of Vertebrate Animals used for
Experimental and other Scientific Purposes (ETS No.
123). Guidelines for Accomodation and care of animals
(Article 5 of the Convention). Council of Europe, Stras-
bourg. Available at:
Cowx, I.G. (1999) An appraisal of stocking strategies in
the light of developing country constraints. Fisheries
Management and Ecology 6,2134.
D’Anna, G., Giacalone, V.M., Vega Fern
andez, T., et al.
(2012) Effects of predator and shelter conditioning
on hatchery-reared white seabream Diplodus sargus
(L., 1758) released at sea. Aquaculture 356357,
Dawkins, M.S. (2006) A user’s guide to animal welfare
science. Trends in Ecology & Evolution 21,7782.
Delaney, M., Follet, C., Ryan, N., Hanney, N., Lusk-
Yablick, J. and Gerlach, G. (2002) Social interaction
and distribution of female zebrafish (Danio rerio)in
a large aquarium. The Biological Bulletin 203, 240
Delicio, H.C., Barreto, R.E., Normandes, E.B., Luchiari,
A.C. and Marcondes, A.L. (2006) A place preference
test in the fish Nile tilapia. Journal of Experimental Ani-
mal Science 43, 141148.
Devlin, R.H., Vandersteen, W.E., Uh, M. and Stevens,
E.D. (2012) Genetically modified growth affects allome-
try of eye and brain in salmonids. Canadian Journal of
Zoology 90, 193202.
Dill, P.A. (1977) Development of behaviour in alevins of
Atlantic salmon, Salmo salar, and rainbow trout, S.
gairdneri.Animal Behaviour 25, 116121.
Dolinsek, I.J., Biron, M. and Grant, J.W.A. (2007a)
Assessing the effects of visual isolation on the popula-
tion density of Atlantic salmon (Salmo salar) using GIS.
River Research and Applications 23, 763774.
Dolinsek, I.J., Grant, J.W.A. and Biron, P.M. (2007b) The
effect of habitat heterogeneity on the population den-
sity of juvenile Atlantic salmon Salmo salar L. Journal
of Fish Biology 70, 206214.
Dou, S., Seikai, T. and Tsukamoto, K. (2000) Cannibal-
ism in Japanese flounder juveniles, Paralichthys olivac-
eus, reared under controlled conditions. Aquaculture
182, 149159.
Eason, P.K. and Stamps, J.A. (1992) The effect of visibil-
ity on territory size and shape. Behavioral Ecology 3,
Einfalt, L.M., Wojcieszak, D.B. and Wahl, D.H. (2013)
Behavior, growth and habitat selection of hatchery es-
ocids reared with artificial vegetation. Transactions of
the American Fisheries Society 142, 345352.
Einum, S. and Fleming, I.A. (2001) Implications of
Stocking : ecological interactions between wild and
released salmonids. Nordic Journal of Freshwater
Research 75,5670.
Ellis, T., Howell, B.R. and Hughes, R.N. (1997) The cryp-
tic responses of hatchery-reared sole to a natural sand
substratum. Journal of Fish Biology 51, 389401.
Emadi, H. (1972) Yolk-sac malformation in Pacific salmon.
MSc thesis, Oregon State University, 84 pages.
Fairhurst, G.D., Frey, M.D., Reichert, J.F., Szelest, I.,
Kelly, D.M. and Bortolotti, G.R. (2011) Does environ-
mental enrichment reduce stress? An integrated mea-
sure of corticosterone from feathers provides a novel
perspective PLoS ONE 6, e17663.
Falagas, M.E., Pitsouni, E.I., Malietzis, G.A. and Pappas,
G. (2008) Comparison of PubMed, Scopus, Web of Sci-
ence, and Google Scholar: strengths and weaknesses.
FASEB Journal 22, 338342.
Falahatkar, B. and Shakoorian, M. (2011) Indications for
substrate preferences in juvenile hatchery-reared great
sturgeon, Huso huso.Journal of Applied Ichthyology 27,
Faleiro, F., Narciso, L. and Vicente, L. (2008) Seahorse
behaviour and aquaculture: how to improve Hippocam-
pus guttulatus husbandry and reproduction? Aquacul-
ture 282,3340.
FAO Food and Agriculture Organization of the United
Nations (2014) The State of World Fisheries and Aqua-
culture: Opportunities and challanges. Food and Agricul-
ture Organization of the United Nations, Rome, 243
pp. Available at:
Fast, D.E., Neeley, D., Lind, D.T., et al. (2008) Survival
comparison of spring chinook salmon reared in a pro-
duction hatchery under optimum conventional and
seminatural conditions. Transactions of the American
Fisheries Society 137, 15071518.
Fischer, P. (2000) An experimental test of metabolic and
behavioural responses of benthic fish species to differ-
ent types of substrate. Canadian Journal of Fisheries and
Aquatic Sciences 57, 23362344.
Flagg, T.A. and Nash, C.E. (1999) A conceptual framework
for conservation hatchery strategies for Pacific salmonids.
National Marine Fisheries Service, Seattle, 54 pp.
Available at:
Freitas, R.H.A. and Volpato, G.L. (2013) Motivation and
time of day affect decision-making for substratum
granulometry in the Nile tilapia Oreochromis niloticus.
Journal of Applied Ichthyology 29, 239241.
Fuss, H.J. and Johnson, C. (1988) Effects of artificial sub-
strate and covering on growth and survival of hatch-
ery-reared coho salmon. The Progressive Fish-Culturist
50, 232237.
Gaignon, J.L. and Prouzet, P. (1982)
Elevage su saumon
Atlantique (S. salar)en
ecloserie: essai d’utilisation de
substrats. Bulletin Franc
ßais de Pisciculture 287,15.
Galhardo, L., Correia, J. and Oliveira, R.F. (2008) The
effect of substrate availability on behavioural and
22 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
physiological indicators of welfare in the African cich-
lid (Oreochromis mossambicus). Animal Welfare 17,
Galhardo, L., Almeida, O. and Oliveira, R.F. (2009) Pref-
erence for the presence of substrate in male cichlid
fish: effects of social dominance and context. Applied
Animal Behaviour Science 120, 224230.
Galhardo, L., Vital, J. and Oliveira, R.F. (2011) The role
of predictability in the stress response of a cichlid fish.
Physiology & Behavior 102, 367372.
no-Paz, M.V., Couderc, S. and Adams, C.E. (2010)
Habitat complexity modulates phenotype expression
through developmental plasticity in the threespine
stickleback. Biological Journal of the Linnean Society
100, 407413.
Gerasimov, Y.V. and Stolbunov, I.A. (2007) Effect of
environmental information richness during early
development of bream (Abramis brama; Cyprinidae)
upon feeding and defensive behavior of its yearlings.
Journal of Ichthyology 47, 246253.
Gessner, J., Kamerichs, C.M., Kloas, W. and Wuertz, S.
(2009) Behavioural and physiological responses in
early life phases of Atlantic sturgeon (Acipenser oxyrin-
chus Mitchill 1815) towards different substrates. Jour-
nal of Applied Ichthyology 25,8390.
Gil, M.M., Palmer, M., Grau, A., Deudero, S., Alconchel,
J.I. and Catal
an, I.A. (2014) Adapting to the wild: the
case of aquaculture-produced and released meagres Ar-
gyrosomus regius.Journal of Fish Biology 84,1030.
Gonda, A., Herczeg, G. and Meril
a, J. (2009) Habitat-
dependent and -independent plastic responses to social
environment in the nine-spined stickleback (Pungitius
pungitius) brain. Proceedings of the Royal Society B 276,
Goosen, K., Ingle-M
oller, R., Doel, D. and van den Ma-
dise, J. (2008) Fish food: assessing foraging opportuni-
ties for Malawi cichlids. The Shape of Enrichment 17,
Gotceitas, V. and Colgan, P. (1989) Predator foraging
success and habitat complexity: quantitative test of the
threshold hypothesis. Oecologia 80, 158166.
Grant, J.W.A. (1997) Territoriality. In: Behavioural Ecol-
ogy of Teleost Fishes, Vol. 28. (ed J.-G.G. Godin). Oxford
University Press, Oxford, pp. 81103.
Grimsrud, K.M., Nielsen, H.M., Navrud, S. and Olesen, I.
(2013) Households’ willingness-to-pay for improved
fish welfare in breeding programs for farmed Atlantic
salmon. Aquaculture 372375,1927.
Gross, M.R. (1998) One species with two biologies:
Atlantic salmon (Salmo salar) in the wild and in aqua-
culture. Canadian Journal of Fisheries and Aquatic Sci-
ences 55, 131144.
Gustafsson, P., Greenberg, L.A. and Bergman, E. (2012)
The influence of large wood on brown trout (Salmo
trutta) behaviour and surface foraging. Freshwater Biol-
ogy 57, 10501059.
Gustafsson, P., Greenberg, L.A. and Bergman, E. (2014)
Woody debris and terrestrial invertebrates effects on
prey resources for brown trout (Salmo trutta) in a bor-
eal stream. Environmental Biology of Fishes 97, 529
Guy, J.H., Meads, Z.A., Shiel, R.S. and Edwards, S.A.
(2013) The effect of combining different environmental
enrichment materials on enrichment use by growing
pigs. Applied Animal Behaviour Science 144, 102107.
Gwak, W.-S. (2003) Effects of shelter on growth and sur-
vival in age-0 black sea bass, Centropristis striata (L.).
Aquaculture Research 34, 13871390.
Hall, S.L. (1998) Object play by adult animlas. In: Animal
Play: Evolutionary, Comparative, and Ecological Perspec-
tives. (eds M. Bekoff and J.A. Byers). Cambridge Univer-
sity Press, Cambridge, pp. 4560.
Hansen, T. (1985) Artificial hatching substrate: effect on
yolk absorption, mortality and growth during first
feeding of sea trout. Aquaculture 46, 275285.
Hansen, T.J. and Møller, D. (1985) Yolk absorption, yolk
sac constrictions, mortality, and growth during first
feeding of Atlantic salmon (Salmo salar) incubated on
astro-turf. Canadian Journal of Fisheries and Aquatic Sci-
ences 42, 10731078.
Hansen, T., Christiansen, R., Nortvedt, R., Stefansson, S.
and Taranger, G.L. (1990) Artificial hatching sub-
strates improve growth and yolk absorption of salmo-
nids. Canadian Technical Report of Fisheries and Aquatic
Sciences 1761,6975.
Hare, V.J., Rich, B. and Worley, K.E. (2008) Enrichment
gone wrong! The Shape of Enrichment Inc., San Diego.
Available at:
Hecht, T. and Appelbaum, S. (1988) Observations on
intraspecific aggression and coeval sibling cannibalism
by larval and juvenile Clarias gariepinus (Clariidae:
Pisces) under controlled conditions. Journal of Zoology
Heggenes, J. and Traaen, T. (1988) Daylight responses to
overhead cover in stream channels for fry of four sal-
monid species. Holarctic Ecology 11, 194201.
Henry, P.-Y., Salgado, C.L., Mun, F.P. and Wikelski, M.C.
(2013) Birds introduced in new areas show rest disor-
ders. Biology Letters 9, 20130463.
Herbert, B.W., Graham, P.A. and Foster, S.D. (2003)
Effects of added shelter and stocking density on growth
of sleepy cod Oxyeleotris lineolatus in ponds. Journal of
the World Aquaculture Society 34, 433440.
Hoelzer, G. (1987) The effect of early experience on
aggression in two territorial scorpaenid fishes. Environ-
mental Biology of Fishes 19, 183194.
Hossain, M.A.R., Beveridge, M.C.M. and Haylor, G.S.
(1998) The effects of density, light and shelter on
the growth and survival of African catfish (Clarias
gariepinus Burchell, 1822) fingerlings. Aquaculture
160, 251258.
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 23
Structural enrichment for captive fish JN
aslund and J I Johnsson
Howell, B.R. and Canario, A.V.M. (1987) The influence
of sand on the estimation of resting metabolic rate of
juvenile sole, Solea solea (L.). Journal of Fish Biology 31,
Huntingford, F., Kadri, S. and Jobling, M. (2012) Intro-
duction: Aquaculture and Behaviour. In: Aquaculture
and Behavior (eds F. Huntingford, M. Jobling and S.
Kadri). Blackwell Publishing Ltd., Chichester, pp.
Huntingford, F.A., Adams, C., Braithwaite, V.A. et al.
(2006) Current issues in fish welfare. Journal of Fish
Biology 68, 332372.
Hutchins, M., Smith, B. and Allard, R. (2003) In defense
of zoos and aquariums: the ethical basis for keeping
wild animals in captivity. Journal of the American Veteri-
nary Medical Association 223, 958966.
Hutchinson, J.M.C. (2005) Is more choice always desir-
able? Evidence and arguments from leks, food selec-
tion, and environmental enrichment. Biological Reviews
arinen, P. and Rodewald, P. (2013) Enriched rearing
improves survival of hatchery-reared Atlantic salmon
smolts during migration in the River Tornionjoki.
Canadian Journal of Fisheries and Aquatic Sciences 70,
arinen, P., Korhonen, P., Leinonen, A. and Hirvonen,
H. (2011) Virikepoikanen p
a paremmin - Stimuler-
ade yngel klarar sig b
attre. Suomen Kalankasvattaja
Fiskodlaren,2011:1,3440. [In Finnish and Swedish.]
oglund, E., Weltzien, F.-A., Schjolden, J., Winberg, S.,
Ursin, H. and Døving, K.B. (2005) Avoidance behavior
and brain monoamines in fish. Brain Research 1032,
o, J., Johnsson, J.I. and Bohlin, T. (2004) Habitat
complexity reduces the growth of aggressive and domi-
nant brown trout (Salmo trutta) relative to subordinates.
Behavioral Ecology and Sociobiology 56, 286289.
Iwama, G.K. (2007) The welfare of fish. Diseases of Aqua-
tic Organisms 75, 155158.
Johansen, R., Knudsen, G. and Smith, A. (2005) Acts and
regulations concerning the care and use of fish in Norwe-
gian research, 1st edn. The Norwegian Reference Centre
for Laboratory Animal Science & Alternatives, Norwe-
gian School of Veterinary Science, Oslo. Available at:
Johnsen, B.O. and Hesthagen, T. (1990) Recapture of
pond- and hatchery-reared brown trout, Salmo trutta
L., released in small streams. Aquaculture Research 21,
Johnsson, J.I. (1993) Big and brave: size selection affects
foraging under risk of predation in juvenile rainbow
trout, Oncorhynchus mykiss.Animal Behaviour 45,
Jonsson, S., Br
as, E. and Lundqvist, H. (1999) Stock-
ing of brown trout, Salmo trutta L.: effects of acclimati-
zation. Fisheries Management and Ecology 6, 459473.
Kadry, V.O. and Barreto, R.E. (2010) Environmental
enrichment reduces aggression of pearl cichlid, Geopha-
gus brasiliensis, during resident-intruder interactions.
Neotropical Ichthyology 8, 329332.
Kalleberg, H. (1958) Observations in a stream tank of
territoriality and competition in juvenile salmon and
trout (Salmo salar L. and S. trutta L.). Report of the
Institute of Freshwater Research Drottingholm 39,55
Kang, D.-Y. and Kim, H.-C. (2012) Relevance of environ-
mental factors and physiological pigment hormones
to blind-side hypermelanosis in the cultured floun-
der, Paralichthys olivaceus.Aquaculture,356357,
Kang, D.-Y. and Kim, H.-C. (2013) Importance of bottom
type and background color for growth and blind-side
hypermelanosis of the olive flounder, Paralichthys oli-
vaceus.Aquacultural Engineering 57,18.
Kato, C.E., Costa, B.N., Cabral, J.N., et al. (2010)
Enhancing the environment for longsnout seahorses.
The Shape of Enrichment 19,12.
Kelley, J.L., Magurran, A.E. and Mac
ıas Garc
ıa, C.
(2006) Captive breeding promotes aggression in an
endangered Mexican fish. Biological Conservation 133,
Kellison, G.T., Eggleston, D.B. and Burke, J.S. (2000)
Comparative behaviour and survival of hatchery-
reared versus wild summer flounder (Paralichthys dent-
atus). Canadian Journal of Fisheries and Aquatic Sciences
57, 18701877.
Kerr, S.J. (2006) An historical review of fish culture, stock-
ing and fish transfers in Ontario, 18652004. Ontario
Ministry of Natural Resources, Petersborough. 154 pp.
+ appendices.
Keshavanath, P., Gangadhar, B., Ramesh, T., van Dam,
A., Beveridge, M.C. and Verdegem, M.C. (2004) Effects
of bamboo substrate and supplemental feeding on
growth and production of hybrid red tilapia fingerlings
(Oreochromis mossambicus9Oreochromis niloticus). Aqua-
culture 235, 303314.
Kihslinger, R.L. and Nevitt, G.A. (2006) Early rearing
environment impacts cerebellar growth in juvenile
salmon. Journal of Experimental Biology 209, 504
Kihslinger, R.L., Lema, S.C. and Nevitt, G.A. (2006) Envi-
ronmental rearing conditions produce forebrain differ-
ences in wild chinook salmon Oncorhynchus
tshawytscha.Comparative Biochemistry and Physiology
Part A: Molecular & Integrative Physiology 145,
Killen, S.S., Marras, S., Metcalfe, N.B., McKenzie, D.J. and
Domenici, P. (2013) Environmental stressors alter rela-
tionships between physiology and behaviour. Trends in
Ecology & Evolution 28, 651658.
Kistler, C., Hegglin, D., W
urbel, H. and K
onig, B. (2011)
Preference for structured environment in zebrafish
24 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
(Danio rerio) and checker barbs (Puntius oligolepis).
Applied Animal Behaviour Science 135, 318327.
Koene, P. (2013) Behavioral ecology of captive species:
using behavioral adaptations to assess and enhance
welfare of nonhuman zoo animals. Journal of Applied
Animal Welfare Science 16, 360380.
Kotrschal, A., Sundstr
om, L.F., Brelin, D., Devlin, R.H.
and Kolm, N. (2012) Inside the heads of David and Goli-
ath: environmental effects on brain morphology among
wild and growth-enhanced coho salmon Oncorhynchus
kisutch.Journal of Fish Biology 81, 9871002.
Kuczaj, S., Lacinak, T., Fad, O., Trone, M., Solangi, M.
and Ramos, J. (2002) Keeping environmental enrich-
ment enriching. International Journal of Comparative
Psychology 15, 127137.
Kushnirov, D. and Degani, G. (1991) Growth perfor-
mance of European eel (Anguilla anguilla) under con-
trolled photocycle and shelter availability. Aquacultural
Engineering 10, 219226.
Kwain, W. and MacCrimmon, H.R. (1969) Further
observations on the response of rainbow trout, Salmo
gairdneri, to overhead light. Journal of the Fisheries
Research Board of Canada 26, 32333237.
Kynard, B., Parker, E. and Horgan, M. (2013) Behavioural
response of Kootenai white sturgeon (Acipenser trans-
montanus, Richardson, 1836) early life stages to gravel,
pebble, and rubble substrates: guidelines for rearing sub-
strate size. Journal of Applied Ichthyology 29, 951957.
Lachance, A.-A., Dutil, J.-D., Larocque, R. and Daigle, G.
(2010) Shelter use and behaviour of juvenile spotted
wolffish (Anarhichas minor) in an experimental context.
Environmental Biology of Fishes 88, 207215.
Langen, E.M.A. (2012) Shoaling preferences in female ze-
brafish (Danio rerio) and the effects of nonapeptides and
environmental enrichment. Masters research internship
thesis, Utrecht University, 44 pages.
Lawler, G.H., Sunde, L.A. and Whitaker, J. (1974) Trout
production in prarie ponds. Journal of the Fisheries
Research Board of Canada 31, 929936.
Lee, J.S.F. and Berejikian, B.A. (2008) Effects of the rear-
ing environment on average behaviour and behaviour-
al variation in steelhead. Journal of Fish Biology 72,
Lema, S.C., Hodges, M.J., Marchetti, M.P. and Nevitt,
G.A. (2005) Proliferation zones in the salmon telen-
cephalon and evidence for environmental influence on
proliferation rate. Comparative Biochemistry and Physiol-
ogy Part A: Molecular & Integrative Physiology 141,
Leon, K.A. and Bonney, W.A. (1979) Atlantic salmon
embryos and fry: effects of various incubation and
rearing methods on hatchery survival and growth. The
Progressive Fish-Culturist 41,2025.
om, L. (2008) Under ytan: en rapport om fiskar och
orbundet Djurens R
att (The Swedish
Animal Rights Association), Stockholm. [In Swedish.]
Lorenzen, K., Leber, K.M. and Blankenship, H.L. (2010)
Responsible approach to marine stock enhancement:
an update. Reviews in Fisheries Science 18, 189210.
Lund, V., Mejdell, C.M., R
ocklinsberg, H., Anthony, R.
and H
astein, T. (2007) Expanding the moral circle:
farmed fish as objects of moral concern. Diseases of
Aquatic Organisms 75, 109118.
Macharia, S.K., Ngugi, C.C. and Rasowo, J. (1998) Compar-
ative study of hatching rates of African catfish (Clarias
gariepinus Burchell 1822) eggs on different substrates.
NAGA, WorldFish Center Quarterly 28,2326.
Manosevitz, M. and Montemayor, R.J. (1972) Interaction
of environmental enrichment and genotype. Journal of
Comparative and Physiological Psychology 79,6776.
Marchetti, M.P. and Nevitt, G.A. (2003) Effects of hatch-
ery rearing on brain structures of rainbow trout, On-
corhynchus mykiss.Environmental Biology of Fishes 66,
Marr, D.H.A. (1963) The influence of surface contour on
the behaviour of trout alevins S. trutta L. Animal
Behaviour 11, 412.
Martins, C.I.M., Galhardo, L., Noble, C., et al. (2012)
Behavioural indicators of welfare in farmed fish. Fish
Physiology and Biochemistry 38,1741.
Maximino, C., Marques de Brito, T., Dias, C.A.G.D.M.,
Gouveia, A. and Morato, S. (2010) Scototaxis as anxi-
ety-like behavior in fish. Nature Protocols 5, 209216.
Mayer, I., Meager, J., Skjæraasen, J.E., Rodewald, P.,
Sverdrup, G. and Fern
o, A. (2011) Domestication
causes rapid changes in heart and brain morphology
in Atlantic cod (Gadus morhua). Environmental Biology
of Fishes 92, 181186.
Maynard, D.J., Flagg, T.A., Iwamoto, R.N. and Mahnken,
C.V.W. (2004) A review of recent studies investigating
seminatural rearing strategies as a tool for increasing
Pacific salmon postrelease survival. American Fisheries
Society Symposium 44, 569580.
McCrimmon, H.R. (1954) Stream studies on planted
Atlantic salmon. Journal of the Fisheries Research Board
of Canada 11, 362403.
McVicar, A.H. (1987) Black patch necrosis of the skin of
Solea solea (L.): the role of sand in prophylaxis and
treatment. Journal of Fish Diseases 10,5963.
McVicar, A.H. and White, P.G. (1982) The prevention
and cure of an infectious disease in cultivated juvenile
Dover sole, Solea solea (L.). Aquaculture 26, 213222.
Mellen, J. and Sevenich MacPhee, M. (2001) Philosophy
of environmental enrichment: past, present, and
future. Zoo Biology 20, 211226.
Mesa, M.G. (1991) Variation in feeding, aggression, and
position choice between hatchery and wild cutthroat
trout in an artificial stream. Transactions of the Ameri-
can Fisheries Society 120, 723727.
Metcalfe, N.B., Valdimarsson, S.K. and Morgan, I.J.
(2003) The relative roles of domestication, rearing
environment, prior residence and body size in deciding
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 25
Structural enrichment for captive fish JN
aslund and J I Johnsson
territorial contests between hatchery and wild juvenile
salmon. Journal of Applied Ecology 40, 535544.
Mikheev, V.N., Pasternak, A.F., Tischler, G. and Wan-
ock, J. (2005) Contestable shelters provoke aggres-
sion among 0+perch, Perca fluviatilis.Environmental
Biology of Fishes 73, 227231.
Miller, R.B. (1954) Comparative survival of wild and
hatchery-reared cutthroat trout in a stream. Transac-
tions of the American Fisheries Society 83, 120130.
Millidine, K.J., Armstrong, J.D. and Metcalfe, N.B. (2006)
Presence of shelter reduces maintenance metabolism of
juvenile salmon. Functional Ecology 20, 839845.
Moberg, O., Braithwaite, V.A., Jensen, K.H. and Salvanes,
A.G.V. (2011) Effects of habitat enrichment and food
availability on the foraging behaviour of juvenile
Atlantic cod (Gadus morhua L). Environmental Biology of
Fishes 91, 449457.
Morice, S., Pincebourde, S., Darboux, F., Kaiser, W. and
Casas, J. (2013) Predator-prey pursuit-evasion games
in structurally complex environments. Integrative and
Comparative Biology 53, 767779.
Mork, O.I., Bjerkeng, B. and Rye, M. (1999) Aggressive
interactions in pure and mixed groups of juvenile
farmed and hatchery-reared wild Atlantic salmon
Salmo salar L. in relation to tank substrate. Aquaculture
Research 30, 571578.
Murray, C.B. and Beacham, T.D. (1986) Effect of incuba-
tion density and substrate on the development of chum
salmon eggs and alevins. The Progressive Fish-Culturist
48, 242249.
Myhre, L.C., Forsgren, E. and Amundsen, T. (2013)
Effects of habitat complexity on mating behavior and
mating success in a marine fish. Behavioral Ecology 24,
Narejo, N.T., Rahmatullah, S.M. and Rashid, M.M.
(2003) Effect of different shelters on growth, survival
and productivity of freshwater mud eel, Monopterus cu-
chia (Hamilton) reared in cemented cisterns of BAU,
Mymensingh, Bangladesh. Pakistan Journal of Biological
Sciences 6, 17531757.
Newberry, R.C. (1995) Environmental enrichment:
increasing the biological relevance of captive environ-
ments. Applied Animal Behaviour Science 44, 229243.
Nguyen, R.M. and Crocker, C.E. (2007) The effects of
substrate composition on foraging behavior and
growth rate of larval green sturgeon, Acipenser mediros-
tris.Environmental Biology of Fishes 79, 231241.
Nikolsky, G.V. (1963) The Ecology of Fishes. Academic
Press Inc., London.
Nordgreen, J., Bjørge, M.H., Janczak, A.M. et al. (2013)
The time budget of Atlantic salmon (Salmo salar) held
in enriched tanks. Applied Animal Behaviour Science
144, 147152.
Nortvedt, R., Hansen, T., Holm, M. and Torrissen, O.J.
(1985) The effect of illumination on alevins of Atlantic
salmon (Salmo salar) and rainbow trout (S. gairdneri),
incubated on different substrates. ICES, Council Meet-
ing/F 27, 36.
NRCNA National Research Council of the National
Academies (2011) Guide for the care and use of labora-
tory animals, 8th edn. The National Academies Press,
Washington, DC. Available on:
aslund, I. (1992) Survival and distribution of pond-
and hatchery-reared 0+brown trout, Salmo trutta L.,
released in a Swedish stream. Aquaculture and Fisheries
Management 23, 477488.
aslund, J., Aarestrup, K., Thomassen, S.T. and Johns-
son, J.I. (2012) Early enrichment effects on brain
development in hatchery-reared Atlantic salmon
(Salmo salar): no evidence for a critical period. Canadian
Journal of Fisheries and Aquatic Sciences 69, 1481
aslund, J., Rosengren, M., Del Villar, D., et al. (2013)
Hatchery tank enrichment affects cortisol levels and
shelter-seeking in Atlantic salmon (Salmo salar). Cana-
dian Journal of Fisheries and Aquatic Sciences 70, 585
Oldfield, R.G. (2011) Aggression and welfare in a com-
mon aquarium fish, the Midas cichlid. Journal of
Applied Animal Welfare Science 14, 340360.
Olesen, I., Alfnes, F., Røra, M.B. and Kolstad, K. (2010)
Eliciting consumers’ willingness to pay for organic and
welfare-labelled salmon in a non-hypothetical choice
experiment. Livestock Science 127, 218226.
Olla, B.L., Samet, C. and Studholme, A.L. (1981) Corre-
lates between number of mates, shelter availability and
reproductive behavior in the Tautog Tautoga onitis.
Marine Biology 62, 239248.
Olla, B.L., Davis, M.W. and Ryer, C.H. (1998) Under-
standing how the hatchery environment represses or
promotes the development of behavioral survival skills.
Bulletin of Marine Science 62, 531550.
Olsson, I.A.S. and Dahlborn, K. (2002) Improving hous-
ing conditions for laboratory mice: a review of “envi-
ronmental enrichment”. Laboratory Animals 36, 243
Ottesen, O.H. and Strand, H.K. (1996) Growth, develop-
ment, and skin abnormalities of halibut (Hippoglossus
hippoglossus L.) juveniles kept on different bottom sub-
strates. Aquaculture 146,1725.
Ottesen, O.H., Noga, E.J. and Sandaa, W. (2007) Effect of
substrate on progression and healing of skin erosions
and epidermal papillomas of Atlantic halibut, Hippoglos-
sus hippoglossus (L.). Journal of Fish Diseases 30,4353.
Parker, S.J., Durbin, A.G. and Specker, J.L. (1990) Effects
of leaf litter on survival and growth of juvenile coho
salmon. The Progressive Fish-Culturist 52,6264.
Peake, S. (1999) Substrate preferences of juvenile hatch-
ery-reared lake sturgeon, Acipenser fulvescens.Environ-
mental Biology of Fishes 56, 367374.
26 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
Peterson, R.H. and Martin-Robichaud, D.J. (1995) Yolk
utilization by Atlantic salmon (Salmo salar L.) alevins
in response to temperature and substrate. Aquacultural
Engineering 14,8599.
Peyraud, C. and Labat, R. (1962) Reactions cardio-respi-
ratoires observ
ees chez la sole au cours de l’ensable-
ment. Hydrobiologia 19, 351356.
Pflugfelder, O. (1952) Weitere volumetrische Untersuch-
uber die Wirkung der Augenextirpation und
der Dunkelhaltung auf das Mesencephalon und die
Pseudobranchien von Fischen. Roux’ Archiv f
ur Ent-
wicklungsmechanik 145, 549560. [In German.]
Phelps, R.P. and Silva De Gomez, A. (1992) Influence of
shelter and feeding practices on channel catfish finger-
ling production. The Progressive Fish-Culturist 54,
Pickering, A.D., Griffiths, R. and Pottinger, T.G. (1987)
A comparison of the effects of overhead cover on the
growth, survival and haematology of juvenile Atlantic
salmon, Salmo salar L., brown trout, Salmo trutta L.,
and rainbow trout, Salmo gairdneri Richardson. Aqua-
culture 66, 109124.
Pigliucci, M. (2001) Phenotypic plasticity: beyond nature
and nurture. John Hopkins Press, Baltimore.
Rabben, H. and Huse, I. (1986) Growth of juvenile hali-
but (Hippoglossus hippoglossus L.) in captivity. ICES CM
1986/F 20, 11.
Rahmah, S., Kato, K., Yamamoto, S., Takii, K., Murata,
O. and Senoo, S. (2013) Improved survival and growth
performances with stocking density manipulation and
shelter availability in bagrid catfish Mystus nemurus
(Cuvier & Valenciennes 1840) larvae. Aquaculture
Research 110. doi: 10.1111/are.12148. In press.
Rajesh, K.M., Shankar, K.M., Mohan, C.V. and Mridula,
R.M. (2008) Growth and resistance to Aeromonas hy-
drophila of Indian major carp, rohu (Labeo rohita)in
cisterns treated with sugarcane bagasse as artificial
substrate. In: Diseases in Asian Aquaculture VI (eds M.G.
Bondad-Reantaso, C. V Mohan, M. Crumlish and R.P.
Subasinghe). Fish Health Section, Asian Fisheries Soci-
ety, Manila, pp. 245258.
Ramos, F.M., Recuero, L.B., Silva, T.V.N., Fujimoto, R.Y.,
Lee, J.T. and Ferreira Torres, M. (2013) Shelter selec-
tion in the Amazonian zebra pleco, Hypancistrus zebra
ucker & Nijissen, 1991 (Siluriformes: Loricariidae):
requirements in rearing conditions. Journal of Applied
Ichthyology 29, 927929.
Rasmussen, J.E., Belk, M.C. and Peck, S.L. (2009) Endan-
gered species augmentation: a case study of alternative
rearing methods. Endangered Species Research 8, 225
Riley, S.C., Tatara, C.P. and Scheurer, J.A. (2005)
Aggression and feeding of hatchery-reared and
naturally reared steelhead (Oncorhynchus mykiss) fry in
a laboratory flume and a comparison with observa-
tions in natural streams. Canadian Journal of Fisheries
and Aquatic Sciences 62, 14001409.
Riley, S.C., Tatara, C.P., Berejikian, B.A. and Flagg, T.A.
(2009) Behavior of steelhead fry in a laboratory
stream is affected by fish density but not rearing envi-
ronment. North American Journal of Fisheries Manage-
ment 29, 18061818.
Ritter, J.A. and MacCrimmon, H.R. (1973) Influence of
environmental experience on response of yearling rain-
bow trout (Salmo gairdneri) to a black and white sub-
strate. Journal of the Fisheries Research Board of Canada
30, 17401742.
Roadhouse, S., Saari, M.J., Roadhouse, D. and Pappas,
B.A. (1986) Behavioral and biochemical correlates of
hatchery rearing methods on lake trout. The Progres-
sive Fish-Culturist 48,3842.
Roberts, L.J., Taylor, J. and Garcia de Leaniz, C. (2011)
Environmental enrichment reduces maladaptive risk-
taking behavior in salmon reared for conservation.
Biological Conservation 144, 19721979.
Roberts, L.J., Taylor, J., Gough, P.J., Forman, D.W. and
Garcia de Leaniz, C. (2009) Night stocking facilitates
nocturnal migration of hatchery-reared Atlantic sal-
mon, Salmo salar, smolts. Fisheries Management and
Ecology 16,1013.
Robertson, A. (1919) Hatching fry in gravel. Transactions
of the American Fisheries Society 48, 146156.
Rodewald, P., Hyv
arinen, P. and Hirvonen, H. (2011)
Wild origin and enriched environment promote forag-
ing rate and learning to forage on natural prey of cap-
tive reared Atlantic salmon parr. Ecology of Freshwater
Fish 20, 569579.
Rose, J.D., Arlinghaus, R., Cooke, S.J. et al. (2014)
Can fish really feel pain? Fish and Fisheries 15,97
Sackett, G.P., Novak, M.F.S.X. and Kroeker, R. (1999)
Early experience effects on adaptive behavior: theory
revisited. Mental Retardation and Developmental Disabili-
ties Research Reviews 5,3040.
Sahu, P.K.K., Jena, J.K.K., Das, P.C.C., Mondal, S. and
Das, R. (2007) Production performance of Labeo cal-
basu (Hamilton) in polyculture with three Indian
major carps Catla catla (Hamilton), Labeo rohita
(Hamilton) and Cirrhinus mrigala (Hamilton) with pro-
vision of fertilizers, feed and periphytic substrate as
varied inputs. Aquaculture 262, 333339.
Saikkonen, A., Kek
ainen, J. and Piironen, J. (2011)
Rapid growth of Atlantic salmon juveniles in captivity
may indicate poor performance in nature. Biological
Conservation 144, 23202327.
Salvanes, A.G.V. and Braithwaite, V.A. (2005) Exposure
to variable spatial information in the early rearing
environment generates asymmetries in social interac-
tions in cod (Gadus morhua). Behavioral Ecology and
Sociobiology 59, 250257.
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 27
Structural enrichment for captive fish JN
aslund and J I Johnsson
Salvanes, A.G.V., Moberg, O. and Braithwaite, V.A.
(2007) Effects of early experience on group behaviour
in fish. Animal Behaviour 74, 805811.
Salvanes, A.G.V., Moberg, O., Ebbesson, L.O.E., Nilsen,
O., Jensen, K.H. and Braithwaite, V.A. (2013) Environ-
mental enrichment promotes neural plasticity and cog-
nitive ability in fish. Proceedings of the Royal Society B
280, 20131331.
Santos, A.F.G.N., Garc
ıa-Berthou, E., Hayashi, C. and
Santos, L.N. (2013) When habitat complexity
increases predation risk: experiments with invasive
and neotropical native fishes. Marine and Freshwater
Research 64, 752760.
Saxby, A., Adams, L., Snellgrove, D., Wilson, R.W. and
Sloman, K.A. (2010) The effect of group size on the
behaviour and welfare of four fish species commonly
kept in home aquaria. Applied Animal Behaviour Science
125, 195205.
Schoener, T.W. (1987) Time budgets and territory size:
some simultaneous optimization models for energy
maximizers. American Zoologist 27, 259291.
Schroeder, P., Jones, S., Young, I.S. and Sneddon, L.U.
(2014) What do zebrafish want? Impact of social
grouping, dominance and gender on preference for
enrichment. Laboratory Animals 110. doi: 10.1177/
0023677214538239. In press.
Schuck, H.A. (1948) Survival of hatchery trout in
streams and possible methods of improving the quality
of hatchery trout. The Progressive Fish-Culturist 10,
Scott, G.W., Hull, S.L. and Rollinson, D.J. (1998) Surface
breaking behaviour in a population of captive rays
Raja: the expression of a need to forage? Aquarium Sci-
ences and Conservation 2, 161169.
Seal, W.P. (1890) On the desirability of the establish-
ment, of great public aquaria in the United States.
Transactions of the American Fisheries Society 19,
Segner, H., Sundh, H., Buchmann, K., et al. (2012)
Health of farmed fish: its relation to fish welfare and
its utility as welfare indicator. Fish Physiology and Bio-
chemistry 38,85105.
Shepherdson, D.J. (2003) Environmental enrichment:
past, present and future. International Zoo Yearbook 38,
Shepherdson, D.J. (1994) The role of environmental
enrichment in the captive breeding and reintroduction
of endangered species. In: Creative Conservation - Inter-
active Management of Wild and Captive Animals (eds
P.J.S. Olney, G.M. Mace and A.T.C. Feistner). Chapman
and Hall, London, pp. 167177.
Shepherdson, D.J., Mellen, J.D. and Hutchins, M. (1998)
Second Nature: Environmental Enrichment for Captive Ani-
mals. Smithsonian Institution Press, Washington, DC.
Shoup, D.E., Carlson, R.E. and Heath, R.T. (2003) Effects
of predation risk and foraging return on the diel use of
vegetated habitat by two size-classes of bluegills. Trans-
actions of the American Fisheries Society 132, 590597.
olander, S. and Wickman, A. (1976) S
Bonniers, Stockholm, Sweden. [In Swedish.]
Skov, C. and Koed, A. (2004) Habitat use of 0+year pike
in experimental ponds in relation to cannibalism, zoo-
plankton, water transparency and habitat complexity.
Journal of Fish Biology 64, 448459.
ık, O., Maciak, M. and Hork
y, P. (2012) Shelter use
of familiar and unfamiliar groups of juvenile European
catfish Silurus glanis.Applied Animal Behaviour Science
142, 116123.
Sloman, K.A., Baldwin, L., McMahon, S. and Snellgrove,
D. (2011) The effects of mixed-species assemblage on
the behaviour and welfare of fish held in home aqua-
ria. Applied Animal Behaviour Science 135, 160168.
Smith, C.J. (2011) Assessment of altered rearing environ-
ment on survival and performance of hatchery-reared trout:
implications for cutthroat trout reintroduction programs.
MSc thesis, Montana State University, 101 pages.
Smith, S. (2006) Environmental enrichment plan for
elasmobranchs at Shark Bay, Sea World, Gold Coast,
Australia. In: Proceedings of the 1st Australasian Regio-
nal Environmental Enrichment Conference, Melbourne,
0102 November-06, pp. 6070.
Spence, R., Magurran, A.E. and Smith, C. (2011) Spatial
cognition in zebrafish: the role of strain and rearing
environment. Animal Cognition 14, 607612.
Sternberg, D. (1988) Trout. The Hunting and Fishing
Library, Cy DeCosse Inc., Minnetonka.
Strand, R. and Finstad, B. (2007) Migratory behaviour
in relation to smolt development and releasing strate-
gies in Atlantic salmon (Salmo salar L.) smolts. Aqua-
culture 273, 277283.
Strand, D.A., Utne-Palm, A.C., Jakobsen, P.J., Braithwa-
ite, V.A., Jensen, K.H. and Salvanes, A.G.V. (2010)
Enrichment promotes learning in fish. Marine Ecology
Progress Series 412, 273282.
Stunz, G.W., Levin, P.S. and Minello, T.J. (2001) Selec-
tion of estuarine nursery habitats by wild-caught and
hatchery-reared juvenile red drum in laboratory meso-
cosms. Environmental Biology of Fishes 61, 305313.
Suboski, M.D. and Templeton, J.J. (1989) Life skills train-
ing for hatchery fish: social learning and survival.
Fisheries Research 7, 343352.
om, L.F. and Johnsson, J.I. (2001) Experience
and social environment influence the ability of young
brown trout to forage on live novel prey. Animal
Behaviour 61, 249255.
om, L.F., Petersson, E., H
o, J., Johnsson, J.I.
and J
arvi, T. (2004) Hatchery selection promotes bold-
ness in newly hatched brown trout (Salmo trutta):
implications for dominance. Behavioral Ecology 15,
Sveier, H. and Raae, A.J. (1992) Optimal timing for first
feeding in Atlantic salmon (Salmo salar L.) alevins;
28 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
effect of different hatching substrates correlated to
growth and RNA and DNA metabolism. Aquacultural
Engineering 11,93106.
Szczepkowski, M. (2009) Impact of selected abiotic and
biotic factors on the results of rearing juvenile stages
of northern pike Esox lucius L. in recirculating systems.
Archives of Polish Fisheries 48, 107147.
orensen, J. (1919) Om kl
ackning och utplantering av
olika fiskslag. Skrifter utgivna av S
odra Sveriges Fiske-
orening,1919:2,6874. [In Swedish.]
Tatara, C.P., Riley, S.C. and Scheurer, J.A. (2008) Envi-
ronmental enrichment in steelhead (Oncorhynchus my-
kiss) hatcheries: field evaluation of aggression,
foraging, and territoriality in natural and hatchery fry.
Canadian Journal of Fisheries and Aquatic Sciences 65,
Tatara, C.P., Riley, S.C. and Scheurer, J.A. (2009)
Growth, survival, and habitat use of naturally reared
and hatchery steelhead fry in streams: effects of an
enriched hatchery rearing environment. Transactions of
the American Fisheries Society 138, 441457.
Taylor, S.G. (1984) Quality of pink salmon (Oncorhyn-
chus gorbuscha) fry incubated from eggs in river gravel
or plastic substrates. Aquaculture 42, 359365.
Tipping, J.M. (1998) Return rates of hatchery-produced
sea-run cutthroat trout reared in a pond versus a stan-
dard or baffled raceway. The Progressive Fish-Culturist
Tipping, J.M. (2001) Adult returns of hatchery sea-run
cutthroat trout reared in a seminatural pond for differ-
ing periods prior to release. North American Journal of
Aquaculture 63, 131133.
Tipping, J.M. (2008) Adult returns of hatchery steelhead
juveniles reared in earthen- and asphalt-bottom ponds.
North American Journal of Aquaculture 70, 115117.
Torrezani, C.S., Pinho-Neto, C.F., Miyai, C.A., Sanches,
F.H.C. and Barreto, R.E. (2013) Structural enrichment
reduces aggression in Tilapia rendalli.Marine and Fresh-
water Behaviour and Physiology 46,18.
Trabelsi, A., Gardeur, J.-N., Teletchea, F. and Fontaine,
P. (2011) Effects of 12 factors on burbot Lota lota (L.,
1758) weaning performances using fractional design
experiment. Aquaculture 316, 104110.
Tuckey, L.M. and Smith, T.I.J. (2001) Effects of photope-
riod and substrate on larval development and substrate
preference of juvenile southern flounder, Paralichthys
lethostigma.Journal of Applied Aquaculture 11,3741.
Turek, J., Rand
ak, T., Hork
y, P. et al. (2010) Post-release
growth and dispersal of pond and hatchery-reared
European grayling Thymallus thymallus compared with
their wild conspecifics in a small stream. Journal of Fish
Biology 76, 684693.
Turek, J., Hork
y, P.,
abek, V., Vel
sek, J., Slav
ık, O. and
ak, T. (2012) Recapture and condition of pond-
reared, and hatchery-reared 1+European grayling
stocked in addition to wild conspecifics in a small river.
Knowledge and Management of Aquatic Ecosystems 405,
Turnbull, J.F. and Kadri, S. (2007) Safeguarding the
many guises of farmed fish welfare. Diseases of Aquatic
Organisms 75, 173182.
Uddin, M.S., Farzana, A., Fatema, M.K., Azim, M.E., Wa-
hab, M.A. and Verdegem, M.C.J. (2007) Technical
evaluation of tilapia (Oreochromis niloticus) monocul-
ture and tilapiaprawn (Macrobrachium rosenbergii)
polyculture in earthen ponds with or without sub-
strates for periphyton development. Aquaculture 269,
Valdimarsson, S.K. and Metcalfe, N.B. (1998) Shelter
selection in juvenile Atlantic salmon, or why do sal-
mon seek shelter in winter? Journal of Fish Biology 52,
van Dam, A.A., Beveridge, M.C.M., Azim, M.E. and Ver-
degem, M.C.J. (2002) The potential of fish production
based on periphyton. Reviews in Fish Biology and Fish-
eries 12,131.
van Praag, H., Kempermann, G. and Gage, F.H. (2000)
Neural consequences of environmental enrichment.
Nature Reviews Neuroscience 1, 191198.
Veasey, J.S., Waran, N.K. and Young, R.J. (1996) On
comparing the behaviour of zoo housed animals with
wild conspecifics as a welfare indicator. Animal Welfare
Vehanen, T. and Huusko, A. (2011) Brown trout Salmo
trutta express different morphometrics due to diver-
gence in the rearing environment. Journal of Fish Biol-
ogy 79, 11671181.
Vincent, R.E. (1960) Some influences of domestication
upon three stocks of brook trout (Salvelinus fontinalis
Mitchill). Transactions of the American Fisheries Society
Vindas, M.A., Folkedal, O., Kristiansen, T.S. et al. (2012)
Omission of expected reward agitates Atlantic salmon
(Salmo salar). Animal Cognition 15, 903911.
Volpato, G.L., Gonc
ßalves-de-Freitas, E. and Fernandes-de-
Castilho, M. (2007) Insights into the concept of
fish welfare. Diseases of Aquatic Organisms 75,
von Krogh, K., Sørensen, C., Nilsson, G.E. and Øverli, Ø.
(2010) Forebrain cell proliferation, behavior, and
physiology of zebrafish, Danio rerio, kept in enriched or
barren environments. Physiology & Behavior 101,32
Wagner, E.J., Ross, D.A., Routledge, D., Scheer, B. and
Bosakowski, T. (1995) Performance and behavior of
cutthroat trout (Oncorhynchus clarki) reared in covered
raceways or demand fed. Aquaculture 136, 131140.
Wagner, E.J., Routledge, M.D. and Intelmann, S.S.
(1996) Fin condition and health profiles of albino rain-
bow trout reared in concrete raceways with and with-
out a cobble substrate. The Progressive Fish-Culturist
©2014 John Wiley & Sons Ltd, F I SH and F I S H E R I E S , 17, 1–30 29
Structural enrichment for captive fish JN
aslund and J I Johnsson
Watters, J.V. (2009) Toward a predictive theory for envi-
ronmental enrichment. Zoo Biology 28, 609622.
Wells, D.L. (2009) Sensory stimulation as environmental
enrichment for captive animals: a review. Applied Ani-
mal Behaviour Science 118,111.
Werner, E.E. and Hall, D.J. (1988) Ontogenetic habitat
shifts in bluegill: the foraging rate-predation risk trade-
off. Ecology 69, 13521366.
Westlund, K. (2014) Training is enrichment and
beyond. Applied Animal Behaviour Science 152,15.
Wilkes, L., Owen, S.F., Readman, G.D., Sloman, K.A. and
Wilson, R.W. (2012) Does structural enrichment for
toxicology studies improve zebrafish welfare? Applied
Animal Behaviour Science 139, 143150.
Williams, T.D., Readman, G.D. and Owen, S.F. (2009)
Key issues concerning environmental enrichment for
laboratory-held fish species. Laboratory Animals 43,
Wiszniewski, G., Duda, A. and Kolman, R. (2010)
Wpływ warunk
ow przetrzymywania larw jesiotra os-
tronosego na ich wzrost i prze_
c. Komunikaty
Rybackie 2,810.
Wocher, H., Hars
anyi, A. and Schwarz, F.J. (2011) Hus-
bandry conditions in burbot (Lota lota L.): impact of
shelter availability and stocking density on growth and
behaviour. Aquaculture 315, 340347.
Wootton, R.J., Handisyde, N. and Rowe, C. (2006) The
effect of cover on food consumption and growth in two
freshwater fish species used in experimental studies.
Animal Welfare 15, 309313.
Young, R.J. (2003) Environmental enrichment for captive
animals. Blackwell Publishing, Oxford.
Zimmermann, E.W., Purchase, C.F. and Fleming, I.A.
(2012) Reducing the incidence of net cage biting and
the expression of escape-related behaviors in Atlantic
cod (Gadus morhua) with feeding and cage enrichment.
Applied Animal Behaviour Science 141,7178.
Zydlewski, G.B., Foott, J.S., Nichols, K., Hamelberg, S.,
Zydlewski, J. and Bj
ornsson, B.T. (2003) Enhanced
smolt characteristics of steelhead trout exposed to
alternative hatchery conditions during the final
months of rearing. Aquaculture 222, 101117.
Supporting Information
Additional Supporting Information may be found
in the online version of this article:
Table S1. (a) Abbreviations used in Table S1b.
(b) Summary of publications on physical environ-
mental enrichment for fish.
Table S2. (a) Abbreviations used in Table S2b.
(b) Summary of publications on incubation sub-
strate treatment for eggs and yolk-sac fry.
Table S3. Bibliography of papers investigating
effects of periphyton substrates on fish.
30 ©2014 John Wiley & Sons Ltd, F I S H and F I S H E R I E S , 17, 1–30
Structural enrichment for captive fish JN
aslund and J I Johnsson
... O enriquecimento afeta vários aspectos da biologia de peixes em cativeiro, como a agressão, o estresse, o gasto de energia, as lesões e a suscetibilidade a doenças (Näslund, Johnsson, 2016). Isso permite o bem-estar dos peixes, ou seja, a boa saúde e as condições f ísicas e psicológicas adequadas. ...
... Diariamente, são observadas as condições de saúde (aspecto f ísico, comportamento, longevidade, doenças, ferimento e má nutrição), de estresse (agentes estressores) e comportamentais (agressividade, medo e apatia), a f im de dar as melhores condições possíveis aos peixes nos recintos. Além disso, atividades de enriquecimento são importantes oportunidades para estudos e experimentos que visam investigar vários componentes de enriquecimento para diferentes espécies (Näslund, Johnsson, 2016). ...
... Additionally, studies have demonstrated the potential benefits of integrating environmental enrichment strategies, such as the addition of natural substrates and refuges, in catfish farming to improve welfare and reduce stress. These strategies have been shown to increase growth rates, reduce aggression, and improve overall welfare, suggesting that incorporating environmental enhancements into aquaculture practices can optimize catfish welfare and productivity [110][111][112]. ...
... The large number of O. niloticus found, allegedly related to the environment of the research station. Water habitats that tend to be murky, have slow currents, and have soft substrate conditions are habitats for O. niloticus [14,15]. The low number of T. pectoralis and A. hyalosoma found from Station V is thought to be due to continuous fishing is a factor that causes reduced catches. ...
Full-text available
The objective of the study was to determine the diversity of fish species found in the Teunom River, Aceh Jaya Regency, Aceh Province. The research was conducted from August 2019 until Juli 2020. This research used an Exploration Method. The research station was determined by purposive sampling based on environmental conditions along river flow. Fish samples were collected using fishing rods, traps, and nets. The results of identification indicate there were 431 individual fish that were divided into 11 families and 16 species. Fish species were commonly found from the family of Cyprinidae with six species namely Labtobarbus hosii, Anematichthys apogon, Rasbora sp., Tor tambroides, Osteochilus kappenii , dan Osteochilus vittatus . The five stations’ diversity index (H’) was classified as low to moderate criterion with a value range of 0,80 to 1,86. The dominance index (C) ranged from 0,17 to 0,52. The evenness index (E) ranged from 0,43 to 0,97. While the similarity index of fish species between stations ranged from 0,0% to 0,89%. The physics-chemical condition of Teunom River water was considered to be optimum for the survival of fish.
... Enrichment activities for fish should be used whenever possible to make the captive environment more stimulating and allow the fish to express natural species-appropriate behaviors. However, due to the wide diversity of fish species in public displays with varying natural histories and different physiological and behavioral traits, a species-specific approach for the various species may be required to adequately provide appropriate enrichment [12,[67][68][69][70]. Examples of enrichment for aquarium fish may include changes in the environment, diet, or social interaction of the fish [71]. ...
Full-text available
A wide variety of fish species have been displayed in public aquariums and zoological collections for over 150 years. Though the issue of pain perception in fish is still being debated, there is no disagreement that negative impacts on their welfare can significantly affect their health and wellbeing. A general description of the basic biological requirements for maintaining fish in captive environments is presented, but species-specific information and guidelines should be developed for the multitude of species being maintained. A combination of behavioral, performance, and physiological indicators can be used to assess the well-being of these animals. Ultimately, the goal for optimizing the welfare of fish should be to provide the best possible environment, husbandry, and social interactions to promote natural species-specific behaviors of the fish in captivity.
... After all, it is rich in food sources. These differences can result in phylogenetic, anatomical, and morphological differences in a population (Näslund and Johnsson 2016). Bali waters become the Indonesian Through-Flow (ITF) route, where the mass flow of water is carried from the Pacific Ocean to the Indian Ocean. ...
Full-text available
Tapilatu ME, Wijayanti DP, Subagiyo, Sembiring A, Yusmalinda NLA, NIngsih EY, Malik MDA, Pertiwi NPD. 2023. Genetic diversity of wedgefishes and guitarfishes at landing sites in east Indonesia using Cytochrome Subunit I (COI). Biodiversitas 24: 3120-3127. Wedgefish and guitarfish are considered endangered and protected by law in Indonesia due to pressure from overexploitation. They are highly exploited because of their economic value. This condition impacts the decline in the number of populations to the value of genetic diversity. This study used mitochondrial DNA to assess the genetic diversity of wedgefishes and guitarfishes which landed in the eastern part of Indonesia. We found Rhynchobatus australiae (Whitley, 1939) to be the most common species (14 out of 26 sequenced samples), with Glaucostegus typus (Bennett, 1830) and Rhinobatos jimbaranensis (Last, White, & Fahmi, 2006) appearing infrequently. COI sequences were obtained from the NCBI database and utilized in the study to compare population differentiation. Among the R. australiae populations, the results showed that the genetic diversity (Hd) values from Papua, Bali, and Lombok were 1.00, 0.67, and 0.75, respectively. In Papua, G.typus populations showed genetic diversity values of 0.90. R. jimbaranensis from Bali showed a genetic diversity of 0.50. Papua populations indicated higher genetic diversity than Bali and Lombok populations. Furthermore, the analyses of pairwise FST values and AMOVA indicated moderate genetic divergence across reference populations of R. australiae and G. typus in this study. Based on this value, a cautious conservation strategy in optimizing fisheries management will be required to limit anthropogenic impacts.
... gravel, sand), plants (artificial or live), or other features (e.g. shelters in form of pipes, caves) 10,11 can decrease aggressive behaviour 12 , impact on anxiety and stress responses 13 and aid the recovery from stressful situations 14 , see 15 for a review. However, other environmental manipulations can also affect group dynamics in fish. ...
Full-text available
When observed in their preferred environments, animals display behavioural changes, such as an increase in resting or a reduction in agonism, suggestive of positive affect and improved welfare. However, most studies focus on the behaviour of individuals or, at most, pairs of animals; even though in group-living animals beneficial environmental changes may impact on how the group behaves as a whole. In this study, we investigated whether experiencing a preferred visual environment affected the shoaling behaviour of zebrafish (Danio rerio) groups. We first confirmed a group preference for an image of gravel placed underneath the base of a tank compared to a plain white image. Second, we observed replicated groups either with or without the preferred (gravel) image present to determine if a visually enriched and preferred environment could elicit changes in shoaling behaviour. We found a significant interaction between the observation time and test condition, with differences in shoaling behaviour reflective of increased relaxation emerging gradually over time in the gravel condition. The findings of this study reveal that experiencing a preferred environment can alter group behaviour, making such holistic changes valuable as potential indicators of positive welfare.
Reduced food availability increases the capture of several fish species, although the mechanisms responsible for how food resources result in increased capture are undefined. Our objective was to quantify the mechanism by which food availability might influence the angling vulnerability of muskellunge ( Esox masquinongy ). We assessed capture rates in the field under different food levels, quantified the behaviors of muskellunge that were either fed or food deprived, and determined if appetite‐related hormones leptin and ghrelin affected fish behavior. Catch rates of fasted muskellunge were more than twice as high as those of fed muskellunge. However, food deprivation and hormonal treatments did not influence laboratory behavior, which suggested that catch rates of food‐deprived muskellunge increased because fish were more receptive to lures. Furthermore, an ecosystem approach should be used to consider forage as a component of management goals.
Coastal lagoons are key ‘transitional’ aquatic environments for biodiversity conservation. Ecological indicators are useful tools for the management of water resources in the European Union. Among different biological communities, fish are a very sensitive tool to assess environmental integrity. Indeed, their parasites can be used as complementary indicators of habitat quality. Yet there is still a deep lack of information on ecological assessment using fish (along with their parasites) for coastal lagoons, particularly for the Iberian Peninsula. The aim of the present study was to assess the use of fish morphology and their parasite communities as ecological indicators of anthropogenic impact within the Mar Menor coastal lagoon (SE Spain), a Mediterranean area of special conservation concern for European/Iberian biodiversity. Fish samples (black‐striped pipefish Syngnathus abaster and marbled goby Pomatoschistus marmoratus ) were collected in August 2022 from the Littoral (high level of nutrient enrichment) and Barrier habitats. Physical status (both external and internal indices), asymmetry (level of developmental instability), parasite load, diversity and life‐cycle complexity were compared between habitat types. Body condition and mainly the health assessment index were better in the Barrier habitat. Except for pectoral fins in pipefish, the fluctuating asymmetry was statistically greater in the Littoral habitat (i.e. with eutrophication leading to poorer fish development). The parasite load was higher in the Littoral habitat for both host fish species. However, the diversity and life‐cycle complexity of parasite communities were statistically lower in the Barrier habitat (a structurally simpler environment) only for gobies. This study demonstrates an elevated potential for certain fish morphological and parasitological traits to be considered as good ecological indicators of environmental health. This could help environmental managers and policy makers to design effective monitoring programmes to detect impacts within valuable areas for conservation, such as the Mar Menor coastal lagoon.