Effects of high-relief structures on cold temperate fish assemblages: A field experiment

This article was downloaded by: [The University Of Melbourne Libraries]On: 15 March 2013, At: 04:09Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK

Marine Biology ResearchPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/smar20

Effects of high-relief structures on cold temperatefish assemblages: A field experimentDan Wilhelmsson a , Saleh A. S. Yahya a b & Marcus C. Öhman aa Department of Zoology, Stockholm University, S-106 91, Stockholm, Swedenb Institute of Marine Sciences, University of Dar es Salaam, P.O. Box 668, Zanzibar,TanzaniaVersion of record first published: 22 Aug 2006.

To cite this article: Dan Wilhelmsson , Saleh A. S. Yahya & Marcus C. Öhman (2006): Effects of high-relief structures oncold temperate fish assemblages: A field experiment, Marine Biology Research, 2:2, 136-147

To link to this article: http://dx.doi.org/10.1080/17451000600684359

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form toanyone is expressly forbidden.

The publisher does not give any warranty express or implied or make any representation that the contentswill be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug dosesshould be independently verified with primary sources. The publisher shall not be liable for any loss, actions,claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly orindirectly in connection with or arising out of the use of this material.

http://www.tandfonline.com/loi/smar20

http://dx.doi.org/10.1080/17451000600684359

http://www.tandfonline.com/page/terms-and-conditions

ORIGINAL ARTICLE

Effects of high-relief structures on cold temperate fish assemblages:A field experiment

DAN WILHELMSSON1, SALEH A. S. YAHYA1,2 & MARCUS C. OHMAN1

1Department of Zoology, Stockholm University, S-106 91 Stockholm, Sweden, 2Institute of Marine Sciences, University of

Dar es Salaam, P.O. Box 668, Zanzibar, Tanzania

AbstractHigh-relief structures may influence the abundance and diversity of reef-associated fish. We conducted a field experiment toinvestigate whether the presence of vertical structures (PVC pipes) affects fish communities on artificial reefs. The effect ofthe height of the structures (1 and 3 m) was also tested. Furthermore, the effects on fish of placing artificial reefs onotherwise featureless bottoms were quantified. Algal and macro-invertebrate colonization of the reefs was also recorded.The experiment was carried out on the west coast of Sweden over a period of 1 year. The vertical structures had a positiveeffect on fish abundance but not on diversity. The height of the structures did not, however, influence the fish communities.Natural as well as urban vertical structures on the seafloor could have a positive effect on local fish abundance. The positiveeffects of artificial reefs on total fish abundance and diversity were immediate. Of the 10 species recorded, two, the blackgoby Gobius niger and the goldsinny wrasse Ctenolabrus rupestris , dominated over the whole survey period. There weresignificant temporal differences in fish abundance, and diversity increased with time.

Key words: Artificial reefs, biodiversity, human disturbance, offshore wind power, reef profile, Sweden

Introduction

An enhanced understanding of the factors regulating

fish assemblages is of paramount importance in

conservation efforts as well as in fisheries manage-

ment. For example, fish communities that proliferate

in association with the seabed are influenced by

bottom composition and structure. This has been

noted in a number of studies in tropical (Jennings

et al. 1996; Chabanet et al. 1997; Ohman &

Rajasuriya 1998; Garpe & Ohman 2003) and

temperate waters (Choat & Ayling 1987; Jones

1988; Anderson 1994), whereas there is a paucity

of such information from cold temperate seas (but

see for example Pihl et al. 1994; Pihl & Wennhage

2002). Different habitat variables, such as structural

complexity (Anderson 1994; Ohman et al. 1998),

substrate composition and habitat heterogeneity

(e.g. Risk 1972; Luckhurst & Luckhurst 1978;

Bouchon-Navaro et al. 1985; Chabanet et al.

1997) have been shown to be important in regulating

demersal (bottom-dwelling) fish assemblages.

Although the results are not conclusive (see for

example Parrish & Boland 2004; Gratwicke &

Speight 2005a), the vertical relief of the substrate

is another factor that has been considered to be of

importance for the abundance and diversity of fish.

For example, fish abundance was positively corre-

lated with the height of bottom structures (relief

height) in a study by Gratwicke & Speight (2005b).

Fish species richness and total abundance were

shown to be saturating functions of reef height and

percentage vertical surface (Patton et al. 1985). The

diversity of heights represented on a reef (‘‘vertical

diversity’’) has been suggested to influence fish

community structure (Helvey & Smith 1985). Also,

vertical relief was one of the most important habitat

factors influencing fish community structure on

some coral reefs in the Caribbean (Lara & Gonzales

1998). Taxon-specific studies on natural bottoms in

tropical and temperate waters have further shown

that, for example, juvenile cod (Gadus morhua),

rockfish (Sebastes spp.), serranids (Serranidae), and

Correspondence: D. Wilhelmsson, Department of Zoology, Stockholm University, S-10691 Stockholm, Sweden. E-mail: dan.

[email protected]

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory,

University of Copenhagen, Denmark

Marine Biology Research, 2006; 2: 136�147

(Accepted 16 February 2006; Printed 6 June 2006)

ISSN 1745-1000 print/ISSN 1745-1019 online # 2006 Taylor & Francis

DOI: 10.1080/17451000600684359

Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

flatfishes (Pleuronectidae) associate with high-pro-

file structures during parts or most of their life cycle

(Gregory & Anderson 1997; Light & Jones 1997;

Stanley et al. 2002; Tupper & Rudd 2002; Johnson

et al. 2003; Cote et al. 2004). A positive correlation

between reef height and fish diversity was found by

Molles (1978), who proposed that the vertical

zonation enhances resource partitioning in fish

communities.

The height of a reef structure may influence local

recruitment of fish larvae. Compared with a low-

profile reef, a vertical formation present throughout

the water column is more likely to be the first solid

substrate encountered by a larvae seeking settlement

areas, even more so for the surface-oriented larvae,

and can thereby enhance local recruitment (Rilov &

Benayahu 2002). Larvae of different fish species have

different vertical distributions during the pelagic

stages, as well as at the time for settlement (Carr

1991; Hair et al. 1994; Leis et al. 2002). The vertical

distribution of fish larvae influences the availability of

physical structures for settlement, and consequently

the reef relief (i.e. the range of depths provided)

influences the composition of fish assemblages re-

cruiting to that reef (Carr 1991). Rilov & Benayahu

(1998), relying on comprehensive studies of pier

pilings, suggested that effective artificial reefs should

be ‘‘high and vertical in orientation with a large

base’’. They further explained that the upper part

would function as a solid fish aggregating device

enhancing recruitment to the whole structure, in-

cluding the benthic section. Concurrently, it was

demonstrated that by increasing the vertical profile of

reefs, by placing prominent structures (such as fish

aggregating devices) in the water column, recruit-

ment of fish to adjacent benthic reefs could be

enhanced (Beets 1989; Brock & Kam 1994).

There is a great variability in the response of

different fishes to the deployment of artificial reefs

(Bohnsack et al. 1991; Grove et al. 1991; Kim et al.

1994). Furthermore, findings from one geographical

area, for example in terms of habitat quality, may not

be applicable for another, as ecological and environ-

mental factors strongly influence the function of an

artificial reef (Baine 2001). No structured experi-

ment on how artificial reefs affect fish in the cold

temperate waters along the Swedish coast, where for

example season is an important factor (Thorman

1986; Pihl & Wennhage 2002), has been published.

The main purpose of this field experiment,

conducted on the west coast of Sweden, was to

investigate whether non-complex high-relief struc-

tures can increase fish abundance and diversity on

benthic reefs. Also, the influence of the height of the

structures on the colonization of fish of benthic reefs

was tested, with the prediction that higher reefs that

cut through a larger part of the water column attract

more fish to the benthic sections than lower reefs. A

second purpose of the study was to examine how a

local fish assemblage on the Swedish west coast

responds to the deployment of complex artificial

reefs on otherwise featureless sand bottoms.

Methods

Study area

The study was carried out between June 2004 and

May 2005, in the vicinity of the island of Langholmen

near Tjarno Marine Biological Laboratory, Sweden

(Figure 1). The shoreline of the area is characterized

by rocky slopes covered by algae, with sandy and

muddy bottoms below the rocky outcrops. The site is a

flat sandy bottom with little relief, except from a few

small low-profile rocky patches. The area is exposed to

the southwest to the Skagerak strait (Figure 1) and the

tidal range is about 0.3 m (Johannesson 1989). The

temperature of the surface water fluctuates between

15�208C in the summer and 0�28C in the winter. The

average salinity is 25�, and covering ice occurs, on

average, every forth year (Aberg 1992).

Experimental design

To investigate the influence of high-profile structures

on fish assemblages, 24 reefs of three different

designs were constructed (Figure 2). The core of

the benthic reefs consisted of a 50 kg parasol footing

made of concrete supported by a 1.4�/1.4 m armour

grid. To achieve structural complexity on the benthic

reefs, the footing was covered with nine roof tiles

(25�/40 cm) placed in two layers in a fan-shaped

manner around the centre. The reef construction

was ca. 1 m in diameter. Small plastic wires were tied

at the corners of a 1 m2 quadrate to demarcate a

standardized survey area for each unit.

On eight of the 24 reefs, the vertical profile was

enhanced using 3 m high PVC pipes (hereafter

referred to as A-reefs). The pipes, that had a

diameter of 0.11 m, were vertically mounted on

the concrete footing. On another eight reefs the

pipes were 1 m high (B-reefs), whereas the remain-

ing eight units constituted only the concrete footing

and tiles (C-reefs). The pipes were kept non-com-

plex and thus provided no refuge for fish. Controls

included surveys of 1 m2 patches of bare sand

bottom, including 1 m of the water column above

the seabed. The deployment of the reef units and the

underwater construction work took place between

12 and 20 June 2004. The experimental reefs (ERs)

were deployed in a grid pattern at depths ranging

between 9 and 13 m, within an area of 10,000 m2

(Figure 3). The units were arranged in a randomized

Effects of high-relief structures on fish assemblages 137

Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

block design to control for potential temporal and

location effects. Each of the three different treat-

ments and one control were represented in a block,

and were each placed haphazardly in the corner

of 20�/20 m quadrates (Figure 3). The distance

between the quadrates was 20 m.

Field methods

Surveys of the fish assemblages around the artificial

reefs were conducted on 21�25 June, 4�6 August,

3�6 October 2004 and 23�26 May 2005. Censuses

followed procedures modified from Sale & Douglas

(1981). A diver recorded the active species hovering

within 1 m above the ER by slowly circling the patch

at a distance of 2 m. The diver then moved closer to

the reef and enumerated fishes on the bottom within

the 1 m2 square. Finally, the benthic reef sections

were searched for cryptic fish. The complete survey

of one reef unit took approximately 5 min. The same

technique was applied in the controls. The top 2 m

of the A-reefs were also examined, although

Figure 2. Description of the experimental reefs. D represents controls on the bare sand bottom.

Figure 1. Map indicating the study area.

138 D. Wilhelmsson et al.

Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

these sections were not included in the quantitative

survey.

Some fishes are particularly difficult to identify to

species level during visual censuses, and the fish are

often displayed only for short periods. To minimize

the risk of inaccurate identifications, species difficult

to identify were grouped together at higher taxo-

nomic levels. The sand goby, Pomatoschistus minutus ,

and common goby, P. microps , were grouped to-

gether as Pomatoschistus spp. Furthermore, the two

species of Cottidae recorded in the area, the sea

scorpion, Taurulus bubalis , and bull-rout, Myoxoce-

phalus scorpius , were recorded as Cottidae. Flatfishes

were identified together as Pleuronectidae. Restrict-

ing recordings of these fishes to genera and family

levels had negligible effects on calculations of

average species richness and diversity, as it was rare

to find more than one representative of a group on a

single reef unit.

Estimates of the general patterns of fouling on

the PVC pipes were made throughout the study. In

the last survey (May 2005), the surface structure of

the reefs was quantitatively recorded using the line

intercept method (English et al. 1994). Recordings

were taken every 10 cm on the horizontal base of the

reef and every 20 cm on the vertical surface.

Data analysis

Two A-reefs were damaged by a storm before the last

survey. All reefs within the two survey blocks affected

were excluded for the repeated measures analyses

described below. These tests were therefore per-

formed using six replicates of each treatment. For

the analyses using Kruskal�Wallis ANOVA and

Mann�Whitney U-test outlined below, eight repli-

cates for each treatment were included for June�October 2004, whereas the analysis of the data from

May was restricted to six replicates per treatment.

Data on total fish abundance, abundance of the

dominant fish species, species richness and diversity

(H?, Shannon�Wiener information function) were

tested for differences among reef types and over

time. Total and species-wise fish abundance were

analysed using two-way repeated measures ANOVA.

The data sets were tested for normality and homo-

genous variances. Although no transformation was

necessary for total fish abundance, the species-wise

data was ln(x�/1) transformed to meet the assump-

tions of ANOVA. To identify differences, post-

hoc tests were performed using Tukey’s honest

significance test.

For the species number and Shannon diversity

index, the data did not assume normality after

transformation, and the non-parametric Friedman

ANOVA and Kruskal�Wallis ANOVA were applied

for the analysis of changes over time and between

reef types, respectively. The frequency of occurrence

of fish on the bare sand patches (D) was low and

comparisons of abundance and diversity between the

ERs and the controls were made using the non-

parametric Mann�Whitney U-test. The disadvan-

tage of multiple testing using Kruskal�Wallis

ANOVA and Mann�Whitney U-test was taken into

consideration in the interpretation of the data.

Results

Fish abundance

In total, 10 fish species were recorded on the ERs

(Table I). Fish densities differed significantly among

reef types (ANOVA, P�/0.004). Post-hoc tests

showed a higher abundance on the ERs with the

vertical pipes (A- and B-reefs) compared with

those without these structures (C-reefs) (Tukeys,

P�/0.007 and P�/0.01, respectively). The differ-

ences in fish numbers were most pronounced in the

last two surveys (Figure 4). There was no difference

between A-reefs (3 m pipes) and B-reefs (1 m pipes)

(Tukeys, P�/0.9). All ERs had higher fish abun-

dance than the controls on the bare sand bottom (D)

at each survey occasion (Mann-Whitney U-test,

PB/0.01) (Figure 4).

The black goby, Gobius niger, and goldsinny wrasse,

Ctenolabrus rupestris, dominated during the whole

survey period across all reef types, making up 58 and

36% of the total number of fish on the ERs. Both G.

niger and C. rupestris were most abundant in October

(Figures 5 and 6). There were significant differences in

abundance of G. niger among reef types (ANOVA, P�/

0.02) with higher numbers of the species on both

Figure 3. Map showing the position of the experimental reefs

within the study area.


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

Table I. Average fish abundance (9/standard deviation) and diversity per 1 m3 (A�/3 m high, B�/1 m high, C�/only a benthic reef, D�/

bare sand bottom) at each survey occasion (n�/8 for June�October and n�/6 for May, for all treatments).

A B C D

June

Cottidae

Ctenolabrus rupestris 1.75 (0.46) 1.38 (1.06) 1.00 (0.53)

Gadus morhua

Gobiusculus flavescens

Gobius niger 4.00 (1.85) 3.38 (1.69) 3.25 (1.67)

Nerophis ophidion

Pholis gunnellus

Pleuronectidae 0.83 (0.46)

Pomatoschistus spp.

Syngnathus typhle 0.13 (0.35)

Total abundance 5.75 (1.83) 4.75 (2.12) 4.38 (1.51) 0.83 (0.46)

Species number 2.00 (0.00) 1.75 (0.46) 2.00 (0.53) 0.83 (0.46)

Shannon diversity 0.59 (0.08) 0.49 (0.30) 0.57 (0.30) 0

August

Cottidae 0.13 (0.35)


Gadus morhua 0.50 (0.93) 0.38 (1.06) 0.50 (1.41)

Gobiusculus flavescens 0.13 (0.36)

Gobius niger 7.75 (2.82) 6.13 (1.36) 5.25 (1.39)

Nerophis ophidion

Pholis gunnellus 0.13 (0.35) 0.13 (0.35)

Pleuronectidae 0.125 (0.35) 0.13 (0.35)

Pomatoschistus spp. 2.50 (3.29)

Syngnathus typhle

Total abundance 12.63 (4.34) 10.25 (2.96) 10.75 (2.80) 2.63 (3.62)

Species number 2.5 (0.76) 2.25 (0.46) 2.38 (0.52) 0.88 (0.64)

Shannon diversity 0.70 (0.27) 0.63 (0.23) 0.76 (0.22) 0.04

October

Cottidae 0.13 (0.35) 0.50 (1.07) 0.13 (0.35)


Gadus morhua 0.13 (0.35)


Gobius niger 10.25 (2.71) 10.25 (1.67) 8.88 (2.42) 0.25 (0.71)

Nerophis ophidion 0.13 (0.35) 0.13 (0.35)

Pholis gunnellus 0.63 (0.74) 0.25 (0.46) 0.38 (0.74)

Pleuronectidae

Pomatoschistus spp. 0.17 (0.41) 0.50 (1.07)

Syngnathus typhle 0.13 (0.35)

Total abundance 16.75 (2.76) 19.25 (3.28) 13.75 (2.49) 0.75 (1.17)

Species number 2.75 (0.89) 2.88 (1.36) 2.50 (0.76) 0.38 (0.52)


May

Cottidae 0.33 (0.52) 0.17 (0.41)


Gadus morhua 0.33 (0.52) 0.17 (0.41)


Gobius niger 4.17 (2.23) 3.67 (1.21) 1.83 (1.33) 0.33 (0.52)

Nerophis ophidion

Pholis gunnellus 0.17 (0.41) 0.17 (0.41) 0.83 (1.17)

Pleuronectidae 0.17 (0.41) 0.17 (0.41)

Pomatoschistus spp. 0.17 (0.41) 0.33 (0.52)

Syngnathus typhle

Total abundance 8.33 (2.42) 7.83 (3.37) 4.5 (1.87) 0.83 (0.41)

Species number 3.00 (0.89) 2.50 (0.84) 2.67 (0.82) 0.83 (0.41)



Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

A- and B-reefs than on C-reefs (Tukeys, P�/0.02 and

PB/0.05, respectively). For C. rupestris, although

differences among reef types were not statistically

significant (ANOVA P�/0.4), average densities were

higher on the reefs with an enhanced vertical profile

than on C-reefs in October and May (Figure 6).

Pomatoschistus spp. dominated in the controls.

Overall fish abundance varied with time (ANOVA,

PB/0.001), with higher abundances in August and

October 2004 than in June 2004 (Tukeys, PB/0.001)

and May 2005 (Tukeys, PB/0.001). No significant

differences were recorded between June 2004 and

May 2005 (Tukeys, P�/0.2). In May, the average fish

abundance on the C-reefs was back to the level at the

start of the experiment, whereas average abundances

on A- and B-reefs remained slightly higher (Figure

4). The temporal changes for both G. niger and C.

rupestris showed significant differences for the same

comparisons as total fish abundance over time.

Taxonomic diversity

In terms of species richness and Shannon diversity

(H?), there was no difference among reef types at any

Figure 4. Average fish abundance for the different experimental units at each survey occasion (A�/3 m high, B�/1 m high, C�/only a

benthic reef, D�/bare sand bottom; n�/8 for June�October, n�/6 for May, for all treatments).

Figure 5. Average number of Gobius niger for the different experimental units at each survey occasion (A�/3 m high, B�/1 m high, C�/only

a benthic reef, D�/bare sand bottom; n�/8 for June�October, n�/6 for May, for all treatments).


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

survey occasion (Kruskal�Wallis, P�/0.50, for all

tests). Time was an important factor though, with

differences in species richness and Shannon diversity

among surveys (Friedman ANOVA, P�/0.003 and

PB/0.001, respectively), treating all ERs as one

group (as there were no differences among reef

types). Both species richness and diversity increased

steadily with time (Figures 7 and 8). In June 2004,

5�9 days after deployment, only three species,

C. rupestris , G. niger and lesser pipefish, Syngnathus

rostellatus , were noted. In August, cottids, gunnel

Pholis gunnellus , two-spotted goby Gobiusculus

flavescens , cod Gadus morhua , and flatfishes (Pleur-

onectidae) were also recorded. The further enhance-

ment of species richness and Shannon diversity in

October and May 2004 was mainly due to an

increase in frequency of occurrence of cottids and

P. gunnellus . All ERs had higher species richness and

Shannon diversity (H?) than the controls on the bare

sand bottom (D) at each survey occasion (Mann�Whitney U-test, PB/0.01) (Figures 5 and 6).

Other observations

In October, young of the years (B/5 cm) (Hillden

1978) composed at least 21% of the recorded

Figure 6. Average number of Ctenolabrus rupestris for the different experimental units at each survey occasion (A�/3 m high, B�/1 m high,

C�/only a benthic reef, D�/bare sand bottom; n�/8 for June�October, n�/6 for May, for all treatments).

Figure 7. Average number of fish species for the different experimental units at each survey occasion (A�/3 m high, B�/1 m high, C�/only

a benthic reef, D�/bare sand bottom; n�/8 for June�October, n�/6 for May, for all treatments).


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

C. rupestris. Otherwise, few juveniles were recorded.

C. rupestris was the only species that was regularly

noted in the water column above the benthic reefs,

although it was still strongly associated with the

bottom sections, frequently seeking shelter among

the tiles. No fish was observed in association with the

PVC pipes above 1.5 m at any survey occasion. Cod

were noted on the ERs in August, October and May.

In August and October 2004 the cod (length

approximately 20 cm) were passing by foraging on

the bottom and around the reefs, whereas in May

2005 (length approximately 30 cm) they were found

under the tiles of the benthic reefs. Schools of horse

mackerel (Trachurus trachurus) were seen passing by

A- and B-reefs in October. Diving eiders (Somateria

mollissima) were observed in the vicinity of the ERs

in October.

Invertebrates and algae

Sparse settlements of hydroids (Hydrozoa) and

bryozoans (Bryozoa) were noted in the first survey,

only 5�9 days after deployment. Visual estimates of

epibiota content showed that in August, approxi-

mately 30% of the surface of the pipes was covered

with hydroids. Another 10% was covered with sea

squirts (Ascidiacea). In October, sea squirts covered

approximately 30%, whereas the hydroid presence

was similar to the August survey. In May, detailed

investigations revealed that the lower 1 m of the PVC

pipes was almost entirely covered with filamentous

red algae, whereas barnacles, Balanus spp., were

growing at the top of some of the B-reefs.

On the top 2 m of the PVC pipes on the A-reefs,

barnacles covered 14.3% [5.39/standard deviation

(SD)], sea squirts covered 4.3% (7.99/SD), and red

algae dominated with 73% (7.69/SD). Separate

stands of hydroids covered the top 20 cm of some

of the A-reefs. Samples taken from the pipes

revealed scattered growth of sea squirts, barnacles,

and anemones (Anthozoa) in the dense algae cover

along the PVC pipes, and allowed the identification

of sea squirts to the species Ascidiella scabra and

Corella parallelogramma and anemones to the species

Sagartiogeton undatus and Metridium senile . Crabs,

such as Cancer pagurus , Carcinus maenas , Liocarcinus

depurator , Hyas araneus , Macropodia rostrata , were

common on the reefs. In May 2005, a lobster

(Homarus gammarus) was found in one of the

A-reefs.

Discussion

Spatial patterns

By adding structures, the habitat is altered and food

content and shelter may change accordingly, which

could influence fish numbers. Such effects have been

reported from various seas where artificial structures

have been placed on the seafloor (Bohnsack &

Sutherland 1985). In this study, we examined how

artificial reefs as well as vertical structures would

influence fish populations in a cold temperate

Figure 8. Diversity (Shannon�Wiener, H?) of fish for the different experimental units at each survey occasion (A�/3 m high, B�/1 m high,

C�/only a benthic reef, D�/bare sand bottom; n�/8 for June�October, n�/6 for May, for all treatments).


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

habitat characterized by a featureless sand bottom.

The results showed that both factors had a positive

local effect on fish densities. However, only two

species were mainly affected as the ERs were

colonized primarily by C. rupestris and G . niger .

C. rupestris is a common shallow-water fish on the

coasts of western Europe, including the Swedish

west coast (Wheeler 1969). The species is described

to be strongly associated with algae cover (Hillden

1981; Gjøsæter 2002). The ERs in the present study

were devoid of algae cover through most of the study

period. The reef units, however, provided holes and

crevices for shelter, which suggests structural com-

plexity in general, rather than specifically algae

cover, to be a habitat feature in favour of C. rupestris .

The size of the benthic sections of the ERs was

similar to the size of their territories on natural reefs

in the area (Hillden 1981). The ERs may also be

attractive due to their isolation from neighbouring

territories, with clear boundaries. Some of the ERs

maintained as many as 10 adult individuals of C.

rupestris , which is higher than recorded on natural

reefs in the area; the male/female ratio within a

territory is commonly 1/1�4 (Hillden 1984).

The other dominant species on the ERs was

G. niger. Fjøsne & Gjøsæter (1996) pointed out

that the habitat preferences described for G. niger are

contradictory, as some authors maintain that the

favoured habitats include dense algae cover and

stones and crevices (e.g. Jansson et al. 1985;

Magnhagen 1988), whereas others emphasize open

sand and muddy bottoms (Wheeler 1969; Muus

et al. 1999). Costello (1992), however, showed that

they could prefer various habitats, ranging from

large boulders to fine mud. Habitat selection may

also vary with season, with a stronger association

with boulders in the winter than in the summer

(Wilkins & Myers 1992). In the present study, G.

niger was always represented on the ERs in densities

far exceeding those of the surrounding sand bottom.

It is further noticeable that compared with surveys of

natural bottoms in the Baltic (Jansson et al. 1985)

and the Irish coast (Costello 1992) the densities on

the ERs were much higher.

Few juveniles of species other than C. rupestris and

G. niger were noted on the ERs. For many species of

fish, recruitment and survivorship are strongly

related to the amount of refuge present (e.g. Shul-

man 1984). For example, the density and height of

vegetation, within which the juveniles can get

protection from predators, are often good predictors

of fish recruitment (Carr 1991; Levin 1993). The

ERs were devoid of algae during most of the study

period. The shelter offered by the tiles was on a scale

more suitable for adult individuals. The prevalence

of facultative piscivores, such as G. niger (Fjøsne &

Gjøsæter 1996) and C. rupestris (Costello 1992;

Fjøsne & Gjøsæter 1996) may also have caused high

mortality rates of juveniles (Shulman 1984; Caley

1993; Tupper & Boutilier 1997). Crabs, common on

the ERs, may also interfere with or prey upon

juveniles of, for example, G. flavescens (Costello

1992).

Temporal patterns

Fish densities varied throughout the study period.

Numbers started to increase during the construction

phase. The rapid colonization of the new reefs by

fish parallels many studies in other parts of the world

(e.g. Stephan & Lindquist 1989; Bortone et al. 1994;

Golani & Diamant 1999). In addition to the sudden

enhancement of shelter availability, the aggregation

may at the early stage have been augmented by the

disturbance of the sediment, making infauna more

available for food. This study was conducted in a

cold temperate environment where fish are greatly

influenced by seasonality (Thorman 1986; Pihl &

Wennhage 2002). Accordingly, the overall fish

abundance fluctuated over time, mainly due to

changes in densities of the dominant G. niger and

C. rupestris . In northern Europe, the abundances of

these species decline nearshore during the autumn

and winter as the adults migrate to deeper waters

(Hillden 1981; Nash 1984; Jansson et al. 1985). In

May, the figures were low, and the fish survey may

have been conducted before their return to the

shallows was completed (Hillden 1981). There

were also some changes in habitat quality over

time, as the vertical structures were covered by

delicate red algae in May.

Influence of vertical structures

The vertical structures (PVC pipes) had a positive

effect on local fish densities. Plankton feeders have

been noticed to associate with vertical structures as it

provides both protection and favourable current

patterns (Rountree 1989; Rilov & Benayahu 1998;

Wilhelmsson et al. 1998, 2006). The structures used

in this study, however, catered primarily for benthic

fish. It has been suggested that reef height has little

or no impact on these categories of fish (Grove &

Sonu 1983; Bohnsack et al. 1991). A study on

artificial reefs that were up to 1 m high, however,

indicated that reef height also influences benthic fish

(Molles 1978). Also, the abundance of demersal fish

was related to reef height up to 0.75 m in a study by

Patton et al. (1985). This concurs with the results of

the present study where the vertical structures had a

positive effect on fish abundance, whereas there was


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

no difference between the A-reefs (3 m) and the B-

reefs (1 m).

The attraction of fish to the high-profile reefs can

be due to a number of reasons. High-relief structures

can function as landmarks for fish orientation (Jessee

et al. 1985). Fish may cue on the erected PVC pipes,

functioning as a kind of fish aggregating device, and

then settle on the benthic reefs, as shown with other

vertical structures in experiments by Beets (1989)

and Brock & Kam (1994). C. rupestris , which

commonly inhabits vertical or sloping rocky bottom

with algae cover, use protruding structures as land-

marks for its territories (Hillden 1981). The ERs

may replace natural structures for this species.

Another possible explanation for higher abundances

on A- and B-reefs involves food availability. The

epibiota on the PVC pipes, including hydroids and

bryozoans, provides C. rupestris with food (Hillden

1978; Fjøsne & Gjøsæter 1996). The decomposition

of organic litter, such as faecal matter and pieces of

dead and live organisms, could also increase the

benthic production on and around the reefs (Bray

et al. 1981; Kellison & Sedberry 1998).

If food availability is an important factor, the

higher A-reefs, which provide larger surfaces for

substrate-associated organic production, could be

expected to generate a larger energy input to the

benthic reefs, and attract more fish. Due to their

higher relief, the A-reefs may also be easier to locate

than the B-reefs. However, there was no difference

in fish abundance between the A- and B-reefs. First,

a large portion of the organic litter falling from the

top 2 m of the A-reefs may be dispersed by currents

and not be deposited on the reefs below. Also, no C.

rupestris was noted more than 1.5 m above the

bottom. C. rupestris probably did not use the upper

portions of the A-reefs for grazing, as the fish would

then find itself too far from the shelter in the benthic

reefs. To speculate further, a high reef could be used

as a landmark for visitors (Jessee et al. 1985).

Piscivores, such as cod, mackerel and diving birds

were noticed around the ERs, and the predation

pressure may have been highest on the A-reefs and

kept the fish numbers down.

Additional support for the significance of reef

height can be derived from studies on urban

structures in the sea that are characterized by high

vertical relief. For example, offshore wind power

plants, cooling-water intakes, oil rigs, pier pilings,

and high-profile shipwrecks seem to concentrate fish

effectively (Helvey & Smith 1985; Stephan &

Lindquist 1989; Wilhelmsson et al. 1998, 2006).

In a study of offshore windmills in the Straight of

Kalmar, Baltic Sea, Wilhelmsson et al. (2006) found

that the densities of fish were comparatively high on

the bottom adjacent to the piles of the windmills.

The habitat structure of the seabed surrounding the

windmills had, however, been altered during the

construction phase and/or over time (2�3 years) as a

secondary effect of the piles. Therefore, it was not

possible to explain the aggregation of the bottom-

dwelling fish as a direct effect of the presence of the

structures alone. In the present experiment, the

habitat structure of the benthic reefs was standar-

dized among treatments. The results show that

vertical structures such as piles placed on the bottom

directly, and also in the relatively short term, may

enhance fish abundance. The influence of vertical

relief on fish communities should be considered

when prioritizing efforts of conservation of marine

habitats. Also, it is worth taking into account when

attempting to predict environmental effects of urban

constructions in the seas, such as pier pilings and

wind power plants.

Acknowledgements

The fieldwork assistance by Sara Hallen, Mans

Rutstrom, Robin Svensson, and Sara Svensson is

acknowledged. We wish to thank the administrative

staff and the researchers at Tjarno Marine Biological

Laboratory for great hospitality and support. We are

also thankful to Dr Nylin for valuable comments on

the manuscript. This study was conducted as part of

the VINDREV project. It was supported by the

Swedish Energy Agency (STEM), Airicole AB

(Sydkraft/E.ON), EU Sixth Framework � the

DOWNVIND project, Goteborg University Marine

Research Centre, Tjarno Marine Biological Labora-

tory and the Sida/SAREC Bilateral Marine Science

Programme between Sweden and Tanzania for

research in marine zoology.

References

.Aberg P. 1992. A demographic study of two populations of the

seaweed Ascophyllum nodosum . Ecology 73(4):1473�87.

Anderson TW. 1994. Role of macroalgal structure in the

distribution and abundance of a temperate reef fish. Marine

Ecology Progress Series 113:279�90.

Baine M. 2001. Artificial reefs: a review of their design, applica-

tion, management and performance. Ocean and Coastal

Management 44:241�59.

Beets J. 1989. Experimental evaluation of fish recruitment to

combinations of fish aggregating devices and benthic artificial

reefs. Bulletin of Marine Science 44(2):973�83.

Bohnsack JA, Johnson DL, Ambrose RF. 1991. Ecology of

artificial reef habitats and fishes. In: Seaman W, Sprague LM,

editors. Artificial Habitats for Marine and Freshwater Fish-

eries. San Diego, California: Academic Press.

Bohnsack JA, Sutherland DL. 1985. Artificial reef research: a

review with recommendations for future priorities. Bulletin of

Marine Science 37(1):11�39.

Bortone SA, Martin T, Bundrick CM. 1994. Factors affecting fish

assemblage development on a modular artificial reef in a


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

northern Gulf of Mexico estuary. Bulletin of Marine Science

55(2�3):319�32.

Bouchon-Navaro Y, Bouchon C, Harmelin-Vivien M. 1985.

Impact of coral degradation on a Chaetodontid fish assem-

blage. Proceedings of the Fifth International Coral Reef

Congress, Tahiti 27 May�1 June. 5: 427�32.

Bray RN, Miller AC, Geesay GG. 1981. The fish connection: a

trophic link between planktonic and rocky reef communities?

Science 214:204�5.

Brock RE, Kam AKH. 1994. Focusing the recruitment of juvenile

fishes on coral reefs. Bulletin of Marine Science 55(2�3):623�30.

Caley MJ. 1993. Predation, recruitment and the dynamics of

communities of coral-reef fishes. Marine Biology 117:33�43.

Carr MH. 1991. Habitat selection and recruitment of an

assemblage of temperate zone reef fishes. Journal of Experi-

mental Marine Biology and Ecology 146:113�37.

Chabanet P, Ralambondrainy H, Amanieu M, Faure G, Galzin R.

1997. Relationships between coral reef substrata and fish. Coral

Reefs 16:93�102.

Choat JH, Ayling AM. 1987. The relationship between habitat

structure and fish faunas on New Zealand reefs. Journal of

Experimental Marine Biology and Ecology 110:257�84.

Costello MJ. 1992. Abundance and spatial overlap of gobies

(Gobiidae) in Lough Hyne, Ireland. Environmental Biology of

Fishes 33:239�48.

Cote D, Moulton S, Frampton PCB, Scruton DA, McKinley RS.

2004. Habitat use and early winter movements by juvenile

Atlantic cod in a coastal area of Newfoundland. Journal of Fish

Biology 64:665�79.

English SC, Wilkinson C, Baker V. 1994. Survey Manual for

Tropical Marine Resources. ASEAN Australian Marine

Science Project. Townsville: Australian Institute of Marine

Science.

Fjøsne K, Gjøsæter J. 1996. Dietary composition and the

potential of food competition between 0-group cod (Gadus

morhua L.) and some other fish species in the littoral zone.

ICES Journal of Marine Science 53:757�70.

Garpe KC, .Ohman MC. 2003. Coral and fish distribution

patterns in Mafia Island Marine Park, Tanzania: fish�habitat

interactions. Hydrobiologia 498:191�211.

Gjøsaeter J. 2002. Distribution and density of goldsinny wrasse

(Ctenolabrus rupestris ) (Labridae) in the Risor and Arendal

areas along the Norwegian coast. Sarsia 87(1):75�81.

Golani D, Diamant A. 1999. Fish colonisation of an artificial reef

in the Gulf of Elat, northern Red Sea. Environmental Biology

of Fishes 54:275�82.

Gratwicke B, Speight MR. 2005a. Effects of habitat complexity on

Caribbean marine fish assemblages. Marine Ecology Progress

Series 292:301�10.

Gratwicke B, Speight MR. 2005b. The relationship between fish

species richness, abundance and habitat complexity in a range

of shallow tropical marine habitats. Journal of Fish Biology

66:650�67.

Gregory RS, Anderson JT. 1997. Substrate selection and use of

protective cover by juvenile cod Gadus Morhua in inshore

waters of Newfoundland. Marine Ecology Progress Series

146:9�20.

Grove RS, Sonu CJ. 1983. Review of Japanese Fishing Reef

Technology. Rosemead: Southern California Edison Co.,

Research and Development Series.

Grove RS, Sonu CJ, Nakamura M. 1991. Design and engineering

of manufactured habitats for fisheries enhancement. In: Sea-

man W, Sprague LM, editors. Artificial Habitats for Marine

and Freshwater Fisheries. San Diego: Academic Press.

Hair CA, Bell JD, Kingsford MJ. 1994. Effects of position in the

water column vertical movement and shade on settlement of

fish to artificial habitats. Bulletin of Marine Science 55(2�3):434�44.

Helvey M, Smith RW. 1985. Influence of habitat structure on the

fish assemblages associated with two cooling-water intake

structures in Southern California. Bulletin of Marine Science

37(1):189�99.

Hillden N-O. 1978. On the feeding of the goldsinny, Ctenolabrus

rupestris L. (Pisces, Labridae). Ophelia 17(2):195�8.

Hillden N-O. 1981. Territoriality and reproductive behavior in the

goldsinny, Ctenolabrus rupestris L. Behavioral Processes

6(3):207�21.

Hillden N-O. 1984. Behavioral Ecology of the Labrid Fishes

(Teleostei: Labridae) at Tjarno on the Swedish West Coast.

Stockholm: University of Stockholm, Department of Zoology

and Tjarno Marine Biological Laboratory.

Jansson B-O, Aneer G, Nellbring S. 1985. Spatial and temporal

distribution of the demersal fish fauna in a Baltic archipelago as

estimated by SCUBA census. Marine Ecology Progress Series

23:31�43.

Jennings S, Boulle DP, Polunin NVC. 1996. Habitat correlates of

the distribution and biomass of Seychelles’ reef fishes. Envir-

onmental Biology of Fishes 46:15�25.

Jessee WN, Carpenter AL, Carter JW. 1985. Distribution patterns

and density estimates of fishes on a Southern California

artificial reef with comparisons to natural kelp-reef habitats.

Bulletin of Marine Science 37(1):214�26.

Johannesson K. 1989. The bare zone of the Swedish rocky shores:

why is it there? Oikos 54:77�86.

Johnson SW, Murphy ML, Csepp DJ. 2003. Distribution, habitat,

and behavior or rockfishes, Sebastes spp., in nearshore waters of

southeastern Alaska: observations from a remotely operated

vehicle. Environmental Biology of Fishes 66:259�70.

Jones GP. 1988. Ecology of rocky reef fish of north-eastern New

Zealand: a review. New Zealand Journal of Marine and Fresh-

water Research 22:445�62.

Kellison TG, Sedberry GR. 1998. The effects of artificial reef

vertical profile and hole diameter on fishes off South Carolina.


Kim CG, Lee JW, Park JS. 1994. Artificial reef designs for Korean

coastal waters. Bulletin of Marine Science 55(2�3):858�66.

Lara NE, Gonzales AE. 1998. The relationship between reef fish

community structure and environmental variables in the south-

ern Mexican Caribbean. Journal of Fish Biology (A) 53:209�21.

Leis JM, Carson-Ewart BM, Webley J. 2002. Settlement behavior

of coral reef fish larvae at subsurface artificial-reef moorings.

Marine and Freshwater Research 53:319�27.

Levin PS. 1993. Habitat structure, conspecific presence and

spatial variation in the recruitment of a temperate reef fish.

Oecologia 94:176�85.

Light PR, Jones GP. 1997. Habitat preference in newly settled

coral trout (Plectropomus leopardus , Serranidae). Coral Reefs

16:117�26.

Luckhurst BE, Luckhurst K. 1978. Analysis of the influence of

substrate variables on coral reef fish communities. Marine

Biology 49:317�23.

Magnhagen C. 1988. Changes in foraging as a response to

predation risk in two gobiid fish species, Pomatoschistus minutus

and Gobius niger . Marine Ecology Progress Series 49:21�6.

Molles MC. 1978. Fish species diversity on model and natural

reef patches: experimental insular biogeography. Ecological

Monographs 48(3):289�305.

Muus BJ, Nielsen JG, Svedberg U. 1999. Havsfisk och fiske i

Nordvasteuropa. Stockholm: Bokforlaget Prisma.

Nash RDM. 1984. Aspects of the biology of the black goby,

Gobius niger L., in Oslofjorden, Norway. Sarsia 69:55�61.


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

.Ohman MC, Rajasuriya A. 1998. Relationships between habitat

structure and fish communities on coral and sandstone reefs.

Environmental Biology of Fishes 53:19�31.

.Ohman MC, Rajasuriya A, Svensson S. 1998. The use of

butterflyfishes (Chaetodontidae) as bio-indicators of habitat

structure and human disturbance. Ambio 27:708�16.

Parrish FA, Boland RC. 2004. Habitat and reef-fish assemblages

of banks in the north-western Hawaiian Islands. Marine

Biology 144:1065�73.

Patton ML, Grove RS, Harman RF. 1985. What do natural reefs

tell us about designing artificial reefs in Southern California?


Pihl L, Wennhage H. 2002. Structure and diversity of fish

assemblages on rocky and soft bottom shores on the Swedish

west coast. Journal of Fish Biology 61:148�66.

Pihl L, Wennhage H, Nilsson S. 1994. Fish assemblage structure

in relation to macrophytes and filamentous epiphytes in shallow

non-tidal rocky and soft bottom habitats. Environmental

Biology of Fishes 39:271�88.

Rilov G, Benayahu Y. 1998. Vertical artificial structures as

an alternative habitat for coral reef fishes in disturbed

environments. Marine Environmental Research 45(4/5):431�51.

Rilov G, Benayahu Y. 2002. Rehabilitation of coral reef-fish

communities: the importance of artificial-reef relief to recruit-

ment rates. Bulletin of Marine Science 70(1):185�97.

Risk MJ. 1972. Fish diversity on a coral reef in the Virgin Islands.

Atoll Research Bulletin 153:1�6.

Rountree RA. 1989. Association of fishes with fish aggregation

devices: effects of structure size on fish abundance. Bulletin of

Marine Science 44:960�72.

Sale PF, Douglas WA. 1981. Precision and accuracy of visual

census technique for fish assemblages on coral patch reefs.

Environmental Biology of Fishes 6:333�9.

Shulman MJ. 1984. Resource limitation and recruitment patterns

in a coral reef fish assemblage. Journal of Experimental Marine

Biology and Ecology 74:85�109.

Stanley RD, Kieser R, Hajirakar M. 2002. Three-dimensional

visualisation of a widow rockfish (Sebastes entomelas ) shoal over

interpolated bathymetry. ICES Journal of Marine Science

59:151�5.

Stephan DC, Lindquist DG. 1989. A comparative analysis of the

fish assemblages associated with old and new shipwrecks and

fish aggregating devices in Onslow Bay, North Carolina.

Bulletin of Marine Science 44:698�717.

Thorman S. 1986. Seasonal colonisation and effects of salinity

and temperature on species richness and abundance of fish of

some brackish and estuarine shallow waters in Sweden.

Holarctic Ecology 9:126�32.

Tupper M, Boutilier RG. 1997. Effects of habitat on settlement,

growth, predation risk and survival of a temperate reef fish.

Marine Ecology Progress Series 151:225�36.

Tupper M, Rudd MA. 2002. Species-specific impacts of a small

marine reserve on reef fish production and fishing productivity

in the Turks and Caicos Islands. Environmental Conservation

29(4):484�92.

Wheeler A. 1969. The Fishes of the British Isles and North West

Europe. London: Macmillan.

Wilhelmsson D, Malm T, Ohman, MC 2006. Influence of offshore

wind power on demersal fish. ICES Journal of Marine Science,

63 available online DOI: 10.1016/j.icesjms.2006.02.007.

Wilhelmsson D, .Ohman MC, Stahl H, Shlesinger Y. 1998.

Artificial reefs and dive tourism in Eilat, Israel. AMBIO

27(8):764�6.

Wilkins HKA, Myers AA. 1992. Microhabitat utilisation by an

assemblage of temperate Gobiidae (Pisces: Teleostei). Marine

Ecology Progress Series 90:103�12.

Editorial responsibility: Tore Høisater


Dow

nloa

ded

by [

The

Uni

vers

ity O

f M

elbo

urne

Lib

rari

es]

at 0

4:09

15

Mar

ch 2

013

Effects of high-relief structures on cold temperate fish assemblages: A field experiment

Documents

Transcript of Effects of high-relief structures on cold temperate fish assemblages: A field experiment