su

n

C

t

Received 12 June 2006; accepted 25 October 2006

cAvailable online 12 December 2006

Abstract

The abundance and size structure of wild fish aggregated around a floating sea-cage fish farm were assessed and compared with control sitesover a period of 1 yr. The farm was located 3.1 km offshore from El Campello (Alicante, SE Spain) and cultivated Sparus aurata and Dicen-trarchus labrax in 14 sea-cages. Fish assemblages were evaluated by visual census using SCUBA on three separate days in each season. On eachsampling day, six 5-min visual counts were made around the cages and six counts were made at control sites, 200 m distant from the farm.Assemblages of wild fish differed greatly between the control sites and the farm, with 12 species observed in farm counts and only 4 in thecontrol counts. Abundance, biomass and diversity were greater in the farm-associated fish assemblage. In most controls, fish were not observed.The most abundant families were Sparidae and Carangidae (>98% of aggregated fish). Assemblages at farms differed among seasons, with Tra-churus mediterraneus dominant during spring, Oblada melanura in summer and Boops boops in autumn and winter. The results indicate greattemporal variability in the farm-associated fish assemblage, which may be related to recruitment periods for juveniles (e.g. O. melanura in sum-mer) and specific preferences by other species for warm (e.g. T. mediterraneus) or cold (e.g. B. boops) water periods. 2006 Elsevier Ltd. All rights reserved.

Keywords: aquaculture; seasonal variability; wild fish; fish culture; visual census; Fish Aggregation Devices (FADs); Mediterranean Sea

1. Introduction

Since the appearance of the first sea-cage fish farms in theearly 1980s, the number of installations has increased dramat-ically in the coastal waters of the Mediterranean Sea (Ferlinand LaCroix, 2000) with hundreds of farms present in Greeceand Spain combined (Theodorou, 1999; Sanchez-Mata andMora, 2000). The two most important species cultured aresea bass (Dicentrarchus labrax) and sea bream (Sparus aur-ata), which are of high importance in European aquaculture.

Due to the extent of sea-cage aquaculture in the Mediterra-nean Sea, numerous studies have evaluated the different im-pacts produced by such installations on the marineenvironment. Studies have documented effects on the watercolumn (Tovar et al., 2000), effects on nearby seagrass com-munities (Delgado et al., 1999; Karakassis et al., 2000), accu-mulation of organic material beneath cages (Karakassis et al.,1998; Heilskov and Holmer, 2001), regeneration of benthicprocesses after the cessation of farming (Karakassis et al.,1999; Mazzola et al., 2000), the effects of sedimentary depo-Temporal variability of wild fia sea-cage fish farm in the so

Carlos Valle a,*, Just T. Bayle-Sempere a

Francisca Gimea Unidad de Biologa Marina, Departamen

Universidad de Alicante, Ap.b SINTEF Fisheries and Aquacul

Estuarine, Coastal and Shelf Scien* Corresponding author.

E-mail address: carlos.valle@ua.es (C. Valle).

0272-7714/$ - see front matter 2006 Elsevier Ltd. All rights reserved.doi:10.1016/j.ecss.2006.10.019h assemblages associated withth-western Mediterranean Sea

, Tim Dempster b, Pablo Sanchez-Jerez a,ez-Casalduero a

to de Ciencias del Mar y Biologa Aplicada,

. 99, E-03080 Alicante, Spain

ure, NO-7465 Trondheim, Norway

e 72 (2007) 299e307www.elsevier.com/locate/ecsssition on benthic organisms (Karakassis and Hatziyanni, 2000;Mazzola et al., 2000; La Rosa et al., 2004) and genetic com-parisons of populations of cultured and wild fish (Alarconet al., 2004). Few studies have investigated wild fish associatedwith aquaculture installations (Dempster et al., 2002;

nDempster et al., 2005) and no study has yet investigated long-term temporal variability of these assemblages.

The aggregative effect of sea-cages on wild fish populationsappears analogous to Fish Aggregation Devices (FADs;Dempster et al., 2002). In this respect, the association of fishwith artificial floating objects has been widely documented(Freon and Dagorn, 2000; Castro et al., 2002), as has the inter-est in using FADs as fishery enhancement tools for fisheries(Dempster and Taquet, 2004). Increased availability of foodunder artificial floating objects and their use as a refugefrom predators (Castro et al., 2002) may explain the attractionof fish to floating structures. Beneath aquaculture installations,greater availability of food exists due to waste feed originatingfrom the cages and faeces from caged fish (Phillips et al.,1985), which enhances the attractive effect of farms (Tuyaet al., 2006) and results in different patterns of presence,abundance and residence of fish in a given area than those ob-served around conventional FADs (Dempster et al., 2002).FADs may also act as recruitment points for some species ofpelagic fish (e.g. Deudero, 2001); no information exists as towhether this occurs around sea-cage fish farms. Accordingto the review by Castro et al. (2002), the majority (>80%)of fish aggregated to FADs are juveniles, whereas Dempsteret al. (2002) found that >80% of fish aggregated around fishfarms were adult.

In spite of the great attraction of fish to sea-cage farms andthe potential for substantial impacts on the distribution andabundance of natural fish populations where farms are wide-spread, few studies have investigated their ecological impactson wild fish. Abundances and biomasses of wild fish areknown to be greater around sea cage farms compared to con-trol localities in Scotland (Carss, 1990), Norway (Bjordal andSkar, 1992), the Canary Islands (Boyra et al., 2004; Tuyaet al., 2005) and the Mediterranean Sea (Dempster et al.,2002, 2005). While numerous studies have documented tem-poral variability of fish populations associated with FADs(Deudero, 2001; Dempster, 2005), no study has yet investi-gated the temporal variability of wild fish assemblages aroundsea cage fish farms over a year in the Mediterranean Sea. Inthis context, the objectives of this study were: (1) to determinethe capacity of a sea-cage farm that cultivated sea bass (Sparusaurata) and sea bream (Dicentrarchus labrax) to attract wildfish; (2) to analyse patterns in the abundance, biomass and di-versity of wild fish associated with the farm over a period of1 yr; and (3) to evaluate the potential of the farm to act as a re-cruitment area for juvenile wild fish.

2. Materials and methods

2.1. Study location

The present study was carried out at a sea bream (Sparusaurata) and sea bass (Dicentrarchus labrax) farm located3.1 km offshore from El Campello (Alicante, Spain) (Fig. 1).

300 C. Valle et al. / Estuarine, Coastal aThe farm was located at a depth of 27e30 m over a bottomconsisting of fine sand and had operated since 1997. Duringthe study, 14 cages of 15 m diameter were in use. The totalsurface area occupied by the farm complex was 71 150 m2.

2.2. Rapid visual counts of fish assemblages

Underwater visual census was used to assess wild fish pop-ulations as they are a fast, non-destructive method that allowsa high degree of replication (Harmelin-Vivien and Harmelin,1975). Wild fish populations at fish farms are particularlysuited to visual census techniques due to the limited diversityof species present at each farm and the lack of cryptic species(Dempster et al., 2002). Further, in environments where large,mobile fish are an important component of the fish assem-blage, visual censuses provide better estimates of abundanceand biomass than other techniques (Harmelin-Vivien andFrancour, 1992).

Rapid visual counts (RVCs) lasting 5-min and coveringa transect volume of 50 m long, 15 m wide and 15 m deepwere made. Total lengths of groups of individuals were re-corded. Counts were carried out at depths oscillating from5e10 m, which allowed all fish between the surface and thebottom of the cage to be recorded. Full details of the methodare described in Dempster et al. (2002). The data obtainedwere introduced into EcoCen (Bayle et al., 2001), where abun-dances and biomasses by species and size distributions werecalculated. Conversions to biomass were carried out usingpublished length-weight relationships from the area of thestudy (Valle et al., 2003). The water temperature wasmeasured daily.

2.3. Experimental design

We tested whether assemblages of fish associated with thefarm would differ from nearby control locations, and whetherassemblage composition would differ among times of the year.The study design incorporated three factors: Impact (farm,control), Season (spring, summer, autumn, winter), and Days(three per season). Impact and season were considered as fixedand orthogonal factors, with a nested factor (Days) on the in-teraction of both. On each sampling day, six replicates werecarried out at the farm location and six at control sites200 m distant from the cages. Prior to ANOVA, heterogeneityof variance was tested with Cochrans C-test. As data werepercentages, they were transformed with arcosen(x 1).ANOVA is robust to heterogeneity of variances, particularlywhen experiments are large and balanced (Underwood, 1997).

2.4. Multivariate analysis

To compare assemblages of fish among seasons and dayswithin seasons, we performed non-metric multivariate analysesusing the PRIMER statistical package (Clarke and Warwick,1994) and the program NPMANOVA (Anderson, 2000). Weused abundance data. Before calculating the Bray-Curtis simi-larity matrix, data were square root transformed to increase

d Shelf Science 72 (2007) 299e307the importance of rare or uncommon species (Clarke, 1993).SIMPER was used to determine the relative importance of

cteS

10

neach species of fish in contributing to the dissimilarity amongsamples or in the similarity among replicates of each group ofsamples. MDS was used to have a graphic representation ofthe results; points that are close together represent samplesthat are very similar in species composition, points that are farapart correspond to very different communities. NPMANOVA(Anderson, 2000) was used to test for significant differencesamong the different factors of the design. In our case, the factorseason was fixed while day was nested.

2.5. Univariate analysis

For univariate analysis, we used a two-factor Analysis ofVariance (ANOVA) with the factors season (fixed) and dayswithin season and test for differences in abundance, biomass,diversity, number of species and abundance in each trophiccategory among. Student-NewmaneKeuls (SNK) tests were

detected. Before analysis, data were tested for homogeneityof the variances with Cochrans test.

We also tested for differences in the size structure of Ob-lada melanura, Diplodus sargus, and Trachurus mediterraneusamong different seasons. For each specie, we looked for themaximum reported length and it was divided between fivesize classes. We used the percentages of representation withineach size class as variables and tested whether this differedamong seasons. In spite of being the most abundant species,the size structure of Boops boops was not analyzed because99.9% of the observed individuals were large (28e36 cm).

3. Results

3.1. Wild fish associated with the fish farm

In total, we estimated 111 208 individuals of 12 fish species

CUDOMAR

20

30

022W024W 018W020W

3826N

3824N

3828N

EL

CAMPELLO

Fig. 1. Location of the fish farm (CUDOMAR) 3.1 km offshore from El Campello on the south-east coast of Spain.Portugal

Fran

Medi

Spain

NORTH

C. Valle et al. / Estuarine, Coastal aapplied apriori if significant differences among seasons weree

rraneanea

301d Shelf Science 72 (2007) 299e307belonging to 6 families (Table 1). All species occurred around

astaeabundance

ofwildfish

per

11250m

3in

cageandcontrolcountsbyseason(m

eanSE).P/D;P:pelagic;D:dem

ersal.TC;Trophic

category;Ma:

macro-carnivore;Me:

meso-carnivore;Mi:micro-

re

Species

P/D

TC

Winter

Spring

Summer

Autumn

Cage

Control

Cage

Control

Cage

Control

Cage

Control

idae

Serioladu

merili

PMa

00

1.71.7

00

04.12.4

0

Trachurus

mediterraneus

PMe

1.80.7

036198

0193

31

0103

0

anthidae

Spicaramaena

PMi

0.10.1

00

00

00

0

idae

Dicentrarchus

labrax

PMa

00

00

1.2

1.1

00.10.1

0

midae

Pom

atom

ussaltator

PMa

00

1.11.1

00

00

0

eBoo

psbo

ops

PMi

50000

10.03.3

00

00

27139

1.11.1

Diplodu

ssargus

DMe

00

00

0.9

0.4

00.80.4

0

Diplodu

svulgaris

DMe

5.64.5

0.40.4

0.60.6

00

00.10.1

0

Oblad

amelan

ura

PMi

139

0125

1.1

1.1

203

35

0133

0

Sparus

aurata

DMe

0.20.1

00.30.2

00.3

0.1

00.20.1

0

Spon

dyliosom

acantha

rus

DMi

1.71.2

00.10.07

00

00.20.1

0

enidae

Sphyraenasphyraena

PMi

2828

03428

05.6

2.6

0.80.8

1.21.1

0

302 C. Valle et al. / Estuarine, CoTable

1

Averag

carnivo

Fam

ily

Carang

Centrac

Moron

Pomato

Sparida

Sphyrathe fish farm while only 4 species were observed during con-trol counts. Sparids were the most species diverse family seen(6 species), with Boops boops (95 075 individuals) and Obladamelanura (4341 individuals) the most abundant species ob-served. Only 243 individuals were counted at control loca-tions, and the majority of control replicates contained no fish(Table 2). The fish farm clearly aggregated higher numbersof fish than the control locations in all four seasons. Themost abundant species in farm counts differed with season;Trachurus mediterraneus dominated in spring (water tempera-ture: 18 C), B. boops in autumn (19 C) and winter (14 C)and O. melanura and T. mediterraneus in summer (26 C).Both the abundance and biomass of wild fish was highest dur-ing winter, while diversity was lowest (Table 2), principallydue to the presence of large schools of B. boops.

3.2. Differences in assemblages among seasons

SIMPER analysis indicated that the percentage of similarityamong winter samples was highest (94.1%), with Boops boopscontributing greatest to the similarity among samples (99.4%).Similarities among samples within autumn (60.9%), spring(60.9%) and summer (65.1%) were also high. The MDS indi-cated clear separation of assemblages at the farm between sea-sons (Fig. 2), with winter and spring counts grouping togetherand separating greatly from summer and autumn counts. Thelow value of stress (0.01) means that the samples do not havea randomly distribution. NPMANOVA detected significant dif-ferences among assemblages between days within seasons( p < 0.001) and seasons ( p < 0.01), indicating that despiteconsiderable variability in assemblages between days withinseasons, aggregations differed significantly among the four sea-sons. This was due mainly to the differences in the abundancesof a few species among seasons (Table 3).Boops boopswas veryabundant in autumn and winter but few occurred during springand summer. In contrast, Trachurus mediterraneus abundanceswere high during spring and summer but it was infrequently ob-served during autumn and winter.Oblada melanurawas presentyear-round, but occurred in far higher abundances during sum-mer, and contributed most to the dissimilarities among summerand the other three seasons. Sphyraena sphyraena also contrib-uted substantially to the dissimilarities among seasons, since itwas more abundant during winter and spring.

3.3. Seasonal variability of the dominant species

ANOVA indicated that abundances of the dominant speciesdiffered significantly among seasons (Boops boops and Obladamelanura ( p < 0.001); Trachurus mediterraneus and Diplodussargus ( p < 0.05); Table 1). Boops boops was highly abundantin winter and autumn but occurred infrequently in spring andsummer. Variability of B. boops between sampling days withinseasons was also high, with significant differences detected forthe factor day ( p < 0.001). T. mediterraneus were significantlymore abundant in spring and summer than winter and autumn,

l and Shelf Science 72 (2007) 299e307and abundances also varied greatly between days ( p < 0.05).O. melanura was common in all seasons, but abundances

r)

dand may be attracted due to this food source. The juvenileO. melanura (

Table 3

Dissimilarities among seasons with respect to abundance of fish associated with the fish farm determined by SIMPER analysis. The most important species with

their percentages of participation are shown. AD: average dissimilarity

B. boops T. mediterraneus O. melanura S. sphyraena D. vulgaris S. aurata S. cantharus S. dumerili D. sargus D. labrax

Win.4 Spr.(AD 98.0)

44.9 35.5 9.85 4.22 2.22 1.54 0.64 0.63 e e

Win.4 Sum.(AD 97.6)

42.0 25.9 25.3 3.74 0.42 0.53 e e 1.06 0.63

Spr.4 Sum.(AD 47.0)

e 32.4 42.9 11.7 3.45 3.35 e 1.17 2.08 1.23

Win.4 Aut.(AD 31.2)

25.3 24.0 29.7 4.33 e 2.60 2.36 5.79 3.41 e

Spr.4 Aut.(AD 81.1)

38.9 32.5 13.9 4.69 2.13 2.23 e 2.57 1.24 e

Sum.4 Aut.(AD 74.8)

39.6 25.3 23.4 4.45 e 1.25 e 2.15 1.95 0.92

cm.

0-12

12.1-

24

24.1-

36

36.1-

48

48.1-

60

Abun

danc

e (av

erage

%)

20

40

60

80

100

0-66.1

-12

12.1-

18

18.1-

24

24.1-

30

Abun

danc

e (av

erage

%)

20

40

60

80

100

0-7.2

7.3-14

.4

14.5-

21.6

21.7-

28.8

28.9-

36

Abun

danc

e (av

erage

%)

20

40

60

80

100a

b

c

cm.

0-33

33.1-

66

66.1-

99

99.1-

132

132.1

-165

Abun

danc

e (av

erage

%)

20

40

60

80

100

0-99.1

-18

18.1-

27

27.1-

36

36.1-

45

Abun

danc

e (av

erage

%)

20

40

60

80

100d

e

304 C. Valle et al. / Estuarine, Coastal and Shelf Science 72 (2007) 299e307Fig. 3. Size frequency distributions of: (a) Boops boops; (b) Oblada melanura; (c) Trachurus mediterraneus; (d) Diplodus sargus; and (e) Sphyraena sphyraenaassociated with the sea-cage fish farm.

nwas considered the determinant factor (Dempster, 2005).However, Boyra et al. (2004) did not find differences inthe wild fish assemblage among 6 sampling times over1 year at 2 fish farms (seabass/seabream) located in theCanary Islands. This major difference in the results of thisstudy and Boyra et al. (2004) may be attributable to thegreater variation in water temperatures among seasons. Tem-peratures varied from 18 to 23 C at the Canary Islands, butranged from 12 to 25 in this study. Temperature stronglyinfluences the composition of fish assemblages in manyenvironments (Madurell et al., 2004). High abundances ofTrachurus spp. in summer around floating objects such asFADs have been observed often (Massuti et al., 1999;Deudero, 2001). Boops boops occurs in coastal watersyear-round throughout the region but only occurred at thefarm in winter and spring when water temperatures werelowest. It is possible they preferred other habitats duringsummer and autumn or that they were displaced by thelarge aggregations of Trachurus mediterraneus. Both speciesexhibit a similar foraging behaviour on lost food pellets un-derneath farms (pers. obs.) and it is possible that they com-pete for this resource.

Oblada melanura, Trachurus mediterraneus and Sphyraneasphyraena were present year-round in certain periods but withsignificant variability in their abundances. Species such asSeriola dumerili, Pomatomus saltator, Spicara maena and S.sphyraena, which were present at the farm sporadically andin relatively low numbers, are migratory or undergo consider-able movements in the coastal zone. They may have appearedat the farm after encountering it during such movements and re-mained in its vicinity for some period as it has ecological cuesthey recognised as belonging to a suitable habitat. In contrast,species such Diplodus sargus and Diplodus vulgaris, whichare less mobile, may have been attracted from nearby habitats.

4.2. Recruitment of juveniles

Recruitment is one of the main responsible factors for attrac-

Winter Spring Summer Autumn

Abun

danc

e (av

erage

%)

20

40

60

80

100 0-6 cm.6.1-12 cm.12.1-18 cm.18.1-24 cm.24.1-30 cm.

Fig. 4. Size frequency distribution for Oblada melanura aggregated at the fish

farm in each season.

C. Valle et al. / Estuarine, Coastal ation of fishes to the farms. Larvae and juveniles of many speciesrecruit to floating objects in coastal waters (Kingsford, 1993).Such structures can mimic other naturally occurring floatingobjects used by fish as habitat until they reach an adequatesize to recruit to adult habitat (Castro et al., 2002). Various fac-tors, which are difficult to distinguish, are likely to affect the re-cruitment of juveniles to fish farms. Reduced risk of predationcan be related to the greater structural complexity of the habitat(Heck and Crowder, 1991), water turbidity (Robertson andBlaber, 1992) and the presence of shadow in these habitats(Helfman, 1981). Oblada melanura exhibited a clear recruit-ment peak during summer, which coincided with its period ofreproduction (Whitehead et al., 1989). After summer, onlylarger sized individuals were present (>24 cm), which indicatesthat either the same fish that recruited as small juvenilesremained around the installation and grew, or that they disap-peared and a second wave of colonisation by larger fishoccurred. This same pattern has been observed over severalyears (Fernandez-Jover et al., unpubl. data). SmallO. melanuraindividuals occur during summer and disappear in winter andspring, perhaps to recruit to nearby habitats since O. melanuradoes not move over great distances in coastal waters.

4.3. Consequences for the management of coastalfisheries

Traditionally, FADs have been utilized as structures to at-tract fish for exploitation (Dempster and Taquet, 2004). Fishfarms attract wild fish in a similar manner to FADs, but thecombination of temporary residence of certain species andthe restriction on fishing inside the farm concession areameans that farms may instead act as small marine protectedareas for demersal and pelagic species (Dempster et al.,2002). Fish observed at farms are mainly adults of large sizeand therefore, with a great reproductive capacity, which maylead to an increase in local fisheries due to export of botheggs and adult biomass into surrounding waters. Export ofadult biomass occurs seasonally, due to the succession of spe-cies throughout the year. This may lead to changes in adjacentfisheries when the most abundant species, such as Trachurusmediterraneus, aggregate to farms or move away. In this sensethere is a recent concept of creating marine protected areas(MPAs) around fish farms (Dempster et al., 2002, 2005). Inspite of the goals of MPAs are incompatible with this kindof industrial activity, they can be ideally suited to the goalof boosting coastal wild fisheries (Dempster et al., 2006).

In this study, the main species that aggregated at the farmwere of relatively low economic importance (e.g. Boops boops,Trachurus mediterraneus, Oblada melanura). However, theirconcentration in large numbers attracts predatory species ofgreater commercial interest, such as Coryphaena hippurus,Seriola dumerili, Pomatomus saltator and Thunnus thynnus(Dempster et al., 2002). The constant supply of high proteinfood when feed is lost through the cages also means that thesebig fish are in better body condition than their wild counterpartselsewhere in the sea (Fernandez-Jover et al., in press). Bettercondition increases the spawning success of fish (Izquierdo

305d Shelf Science 72 (2007) 299e307et al., 2001). In recent years, we have observed a steep increasein commercial and recreational fishing around the limits of the

nfarm concession (pers. obs.), suggesting the fish farm increasesthe catchability of these predatory species. Further studies arerequired to determine the extent of this effect and if it contrib-utes to overfishing of these heavily exploited species.

Acknowledgements

We are grateful to Cudomar company, who gave us accessand provided boat time for the study.

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Temporal variability of wild fish assemblages associated with a sea-cage fish farm in the south-western Mediterranean SeaIntroductionMaterials and methodsStudy locationRapid visual counts of fish assemblagesExperimental designMultivariate analysisUnivariate analysis

ResultsWild fish associated with the fish farmDifferences in assemblages among seasonsSeasonal variability of the dominant speciesSize structure of the dominant species

DiscussionSeasonal variability of wild fish assemblages associated to the fish farmRecruitment of juvenilesConsequences for the management of coastal fisheries

AcknowledgementsReferences