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

February 2016
Fish and Fisheries 17(1):1-30

DOI:10.1111/faf.12088

Authors:

Joacim Näslund

Swedish University of Agricultural Sciences

Jörgen Ingemar Johnsson

University of Gothenburg

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.

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).

…

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.

…

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Environmental enrichment for ﬁsh 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

Abstract

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

Correspondence:

Joacim N€

aslund

Department of

Biological and

Environmental

Sciences, University

of Gothenburg, Box

463, Gothenburg,

SE-405 30, Sweden

Tel.: +46317863696

Fax:

+46 31 41 67 29

E-mail: joacim.

naslund@bioenv.

gu.se

Received 13 Apr

2014

Accepted 25 Jun

2014

Introduction 2

Background 2

Aims and methods 3

Deﬁnition of environmental enrichment 3

Goals of environmental enrichment programs for ﬁsh 4

Welfare 4

Food production 5

Fisheries and conservation management 5

Research 6

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 ﬁsh perform better? 16

Preferences: what do the ﬁshes actually want? 17

General considerations for environmental enrichment research in ﬁsh 17

Concluding remarks 18

Acknowledgements 19

References 19

Supporting Information 30

Introduction

‘[...] 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

Background

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

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 S1–S3, 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

Incubation

Substrates

Salmoniformes

Perciform es

Pleuronectiformes

Cypriniformes

Gadiformes

Siluriformes

Cyprinodontiformes

Gasterosteiformes

Synbranchiformes

Acipenseriformes

Anguilliformes

Atheri niformes

Characiformes

Esociformes

Scorpaeniformes

Characiformes

Salmoniformes

Acipenseriformes

Anguillliformes

Siluriformes

Perciform es

Cypriniformes

Siluriformes

Mugiliformes

Gonorhynchiformes

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).

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 ﬁsh

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.

Welfare

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

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

% of papers

Yes

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.

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

approach.

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

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.

Research

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.

2009).

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€

olander

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€

ojesj€

oet al. 2004). Complexity may

also affect foraging rate, either negatively due to

decreased activity from sheltering, lowered

manoeuvrability or reduced prey detectability

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-

du~

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

1988).

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



ık

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-

diture.

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

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

(N€

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-

ment.

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€

aslund

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

below).

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

2000).

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€

aslund

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

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.

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€

aslund

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-

dependent.

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

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

unpredictability

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

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€

ann€

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;

N€

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;

Alan€

ar€

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;

Benha

€

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€

ar€

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

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

depletion.

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.

2003).

Potentially negative effects of incubation sub-

strates include increased risk of fungal infections

due to food particles being trapped in the sub-

strates (Alan€

ar€

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

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,

Structural enrichment for captive ﬁsh JN

€

aslund and J I Johnsson

but the ﬁsh did not interact much with these

objects.

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€

ari-

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

enrichment

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-

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€

aslund

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

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

enrichment

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.

2003).

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 ﬁsh perform

better?

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

(Hyv€

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

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 ﬁshes 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-

nha

€

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 ﬁsh

Shepherdson (2003) listed four steps for a success-

ful EE strategy: (i) compare wild and captive

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

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.

Acknowledgements

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.

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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.

Structural enrichment for captive ﬁsh JN

€

aslund and J I Johnsson

Environmental enrichment for fish in captive environments: effects of physical structures and substrates - Electronic supplement: TableS1-S3

Data

February 2016

Joacim Näslund · Jörgen Ingemar Johnsson

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Fish welfare

Chapter

Jan 2023

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

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