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Estuarine, Coastal and Shelf Science 109 (2012) 1e10

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Estuarine, Coastal and Shelf Science

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Relationships between fish, sea urchins and macroalgae: The structure of shallowrocky sublittoral communities in the Cyclades, Eastern Mediterranean

Sylvaine Giakoumi a,*, Emma Cebrian b, Giorgos D. Kokkoris a, Enric Ballesteros c, Enric Sala c,d

aDepartment of Marine Sciences, University of the Aegean, University Hill, Mytilene, Lesvos Island 81100, GreecebUniversitat de Girona, Facultat de Ciències, Departament de Ciències Ambientals, Campus Montilivi, 17071 Girona, SpaincCentre d’ Estudis Avançats de Blanes-CSIC, Accés Cala Sant Francesc 14, 17300 Blanes, Girona, SpaindNational Geographic Society, 1145 17th St NW, Washington, DC 20036, USA

a r t i c l e i n f o

Article history:Received 22 November 2010Accepted 19 June 2011Available online 24 June 2011

Keywords:algaebiomassfishoverfishingsea urchinsEastern MediterraneanAegean SeaCyclades Archipelago

* Corresponding author.E-mail address: sylvaine@marine.aegean.gr (S. Gia

0272-7714/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.ecss.2011.06.004

a b s t r a c t

Historical overfishing is the most likely explanation for the depletion of the shallow sublittoralcommunities in many areas not least in the Cyclades Archipelago, Greece. The present study is the firstquantitative study of the shallow rocky sublittoral of the Cyclades based on in situ underwater surveys ofalgal cover, and fish and sea urchin abundance at 181 sampling sites in 25 islands to provide a baselineand investigate the relationship between these communities. Algal turf was the most abundant algalfunctional group, and canopy algae of the genus Cystoseira were more abundant at the northern islands.A range in fish biomass of almost two orders of magnitude was found across islands, but overall theCyclades displayed much lower values than fished areas of the Western Mediterranean. We observedapex predators only in 25% of our sampling sites, and their biomass was uncorrelated to total fishbiomass, indicating a depleted ecosystem. Sea urchin biomass was also low but similar to values found inother Mediterranean islands and was positively correlated with barrens. We observed a gradient ofbenthic community complexity from sea urchin barrens to communities dominated by Cystoseira spp.There was no correlation between sea urchins and their predators Diplodus spp., which presentedextremely low densities.

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1. Introduction

Widespread loss of canopy-forming algae is reported to occuracross many parts of the world’s coastlines and it seems to bedriven by urbanisation, pollution and coastal development (Stenecket al., 2002; Thibaut et al., 2005; Airoldi and Beck, 2007; Connellet al., 2008; Mangialajo et al., 2008) but also increased herbivory(McClanahan and Sala, 1997; Steneck et al., 2002). The transitionfrom macroalgal beds to overgrazed rocky bottoms with corallinealgae has been described thoroughly in shallow sublittoraltemperate (Verlaque, 1987; Andrew and Underwood, 1993; Salaet al., 1998) and tropical ecosystems (Hay, 1984; McClanahan andKurtis, 1991; Jackson, 2001).

Shallow sublittoral rocky reefs from theMediterranean Seaweretypically dominated by canopy-forming algae of the genus Cys-toseira (Giaccone and Bruni, 1973; Thibaut et al., 2005) and abun-dant littoral fishes, as shown in no-take reserves (e.g., Guidetti andSala, 2007). Cystoseira species act as ecosystem engineers in benthic

koumi).

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sublittoral Mediterranean assemblages and are of paramountecological importance (Sales and Ballesteros, 2009), accounting formost of the biomass and production of the shallow benthic algalassemblages (Ballesteros, 1992).

Because of the combined effects of natural events (such ascurrents and seasonal storms) and anthropogenic stressors (such asoverfishing and pollution), many Mediterranean localities havesuffered a shift from abundant fish assemblages and macroalgalbeds to sea urchin barrens (Verlaque, 1987; Sala et al., 1998).Furthermore, rocky bottom mobility, due to natural and human-induced causes, prevents the recovery of canopy-forming algaeand facilitates the establishment of opportunistic species (PerkolFinkel and Airoldi, 2010). The expansion of sea urchin barrens inthe Mediterranean Sea has led to a series of studies on the rela-tionships between predatory fishes, sea urchins and algal assem-blages (e.g. Sala et al., 1998; Ruitton et al., 2000; Micheli et al., 2005;Guidetti, 2006; Hereu et al., 2008). Most of these studies tested thetrophic cascade hypothesis, i.e. whether a decrease in predatoryfish biomass due to overfishing increases sea urchin density, whichin turn reduces the abundance of erect algae. Some of these studiescompared no-take marine reserves and adjacent fished areas. Their

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e102

results showed that trophic cascades do occur but they are notalways the rule (Cardona et al., 2007) or that some prerequisites arenecessary for the indirect effects of fishing to take place (Micheliet al., 2005; Guidetti and Sala, 2007). An essential requisite is thatthe abundance of sea urchin predatorsmust be above a threshold sothat top-down control is in effect; below that abundance, predationpressure is weak and thus trophic cascades are not realized(Guidetti and Sala, 2007). However, these studies were restricted tothe Central and Western Mediterranean, which exhibit nutrientconditions very different from the ultra-oligotrophic EasternMediterranean Basin (Coll et al., 2010).

Here, we provide the first quantitative assessment of fish andbenthic communities and their relationships in the Aegean Sea. Ourobjective was to provide a quantitative baseline and explorewhether ecological interactions described for Western Mediterra-nean shallow rocky bottom assemblages also apply in the EasternMediterranean.

2. Methods and materials

2.1. Study area

The study area was located in the Cyclades Archipelago, CentralAegean, North-Eastern Mediterranean Sea. A total of 181 sites from25 islands with rocky bottoms (Fig. 1) were sampled in JulyeAugust2007 and JuneeJuly 2008. The Aegean Sea is characterized by clear,warm, oligotrophic waters (SoHelME, 2005). The region has beenfished for thousands of years and overfished particularly in the last

Fig. 1. Study area in the Cyclades Archipelago. The

century (Stergiou et al., 1997). In the Cyclades, the fishing fleetconsists mainly of small artisanal fishing boats that use trammelnets and long lines. There are also a few purse seiners and trawlersthat are not allowed to fish in coastal waters closer than 300 m and1.5 nautical miles from shore, respectively. Currently, no marineprotected areas exist in the region. From late spring to early autumn(May to September) the area receives a large number of touriststhat increases the population of the most developed islands by asmuch as five times (Voivontas et al., 2003). This has resulted inuncontrolled coastal development, habitat degradation and anincreased demand for fish and seafood.

2.2. Estimation of cover of benthic groups

At each site, we estimated the cover of different algal taxa/groupusing ten replicate photoquadrats, randomly situated at 3 m depth.A Canon G7 camera was mounted on a 50 � 50 cm frame witha custom-built camera setup. The setup ensured accurate posi-tioning of the camera over the scenes and kept the focal distanceand sampling area fixed. Algae inside each photoquadrat wereidentified visually in the field, at the species level (case of Fucales)or at a rough morphological group level (see next paragraph), andnoted on waterproof paper sheets. Voucher specimens of algaewere collected and preserved. We estimated the percentagecoverage of the algal groups using the software Photogrid 1.0 beta(Preskitt et al., 2004).

The algae identified in the field were attributed to the followinggroups: crustose coralline algae (CCA), turf (small filamentous

181 sampling sites are indicated with the dots.

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e10 3

algae), Cystoseira spp., Sargassum spp., non-calcareous Dictyotales(e.g. Dictyota fasciola, Dictyota implexa), calcareous Dictyotales (e.g.Padina pavonica), Caulerpa prolifera, and alien species includingCaulerpa racemosa var. cylindracea, Stypopodium schimperi andAsparagopsis taxiformis. In addition to algae, we included someother categories in the photo analysis: bare rock, sand, pebbles,seagrass Posidonia oceanica, seagrass Cymodocea nodosa and mac-roinvertebrates (e.g. sponges, bryozoans, tunicates).

2.3. Sea urchin counts and biomass

We estimated sea urchin abundance by counting andmeasuringthe sea urchins Paracentrotus lividus and Arbacia lixula found insideten haphazardly placed 50� 50 cm quadrats at each site. Sea urchinsampling was also conducted at 3 m depth. We measured their testdiameter with a plastic calliper. For analysis, we grouped into 1-cmsize classes (Sala and Zabala, 1996) and then size-frequencydistributions of sea urchins were calculated for each island(Guidetti, 2006).

To estimate the sizeeweight relationships we collected 30 seaurchins of each species, stored in seawater and transported to thelaboratory, wherewemeasured the test diameter of each individualwith a plastic calliper and weighed them on a digital scale. We usedthat wet weight/size relationships to calculate sea urchin biomassat each site.

2.4. Fish counts and biomass

At each site, we conducted standard underwater surveys of theabundance and size of fishes along visual transects. At eachsampling site we conducted three replicate 25� 5 m belt transects,placed parallel to the shore at approximately 3 m depth. Theobserver snorkeled at constant speed, identifying, counting andestimating the size of all individuals within 2.5 m on either side ofthe transect line (La Messa and Vacchi, 1999). We assigned fish taxato functional groups based on published data on diet and trophiclevel (http://www.fishbase.org): zooplanktivores, herbivores,carnivores and apex predators (Guidetti and Sala, 2007).

Length estimates of fish from surveys were converted to wetweight by using the allometric lengtheweight conversion: W ¼ aLb, where W is weight in grams and L is total length in cm.Parameters a and b are constants obtained from Fishbase (Froeseand Pauly, 2009) and Moutopoulos and Stergiou (2002). Wherevalues for a and b were unavailable, the parameters from a conge-neric species with similar shape and maximum total length wereused. We chose the parameter values that corresponded to ourstudy area or to the closest geographical area (Appendix: Table A).

2.5. Data analysis

We investigated correlations among 1) the biomass of largefunctional groups and sea urchins, and 2) herbivore biomass (i.e.sea urchins, Sparisoma cretense, Sarpa salpa and Siganus luridus) andalgal functional groups, using Spearman’s rank of order test (whichdoes not assume bivariate Normality) (SPSS v.17.0). Multivariatepatterns on shallow sublittoral macrobenthic and fish communitieswere visualized using non-metric multidimensional scaling (MDS)ordination (Kruskal and Wish, 1978) based on the BrayeCurtissimilarity matrix calculated from biomass (for fish trophic groupsand sea urchins) and percent cover (for algae) data. We performedan MDS analysis for all sites and another analysis for islands. Takinginto account the large number of sites, MDS ordination (2-dimensional) generated a good fit to the observed data, withstress value below 0.2. A hierarchical group average agglomerativeclustering method accompanied by SIMPROF test (Clarke et al.,

2008) (9999 permutations, 0.1% significance level; Potter et al.,2001) was used to explore potential grouping structures amongsamples. SIMPER analysis was conducted to assess the contributionof the different species to the average BrayeCurtis dissimilaritybetween SIMPROF groups.We used software Primer v.6 (Clarke andGorley, 2006) for the multivariate analysis.

Non-parametric analysis of variance PERMANOVA (Anderson,2001a) was used to test for spatial variability. We applied a hierar-chical design with 2 factors: Island as a random factor and Site asa random factor nested in Island. Tests of significance were basedon 9999 permutations of residuals under a reduced model(Anderson, 2001b; Anderson and ter Braak, 2003).

3. Results

We identified fishes from 47 species belonging to 15 families.We also recorded fishes from another 5 families (Mugilidae, Athe-rinidae, Blennidae, Gobiidae and Tripterygiidae) which were notidentified to the species level (Appendix: Table B). Total fishbiomass ranged from 0.02 to 1.67 kg 125 m�2 across sites, witha mean value of 0.26 kg 125 m�2. At the island level, total fishbiomass ranged from 0.06 (in Strogylo) to 0.56 kg 125 m�2 (inSantorini), with amean value of 0.23 kg 125m�2 (Fig. 2a). However,the low biomass values in Strogylo should be considered withcaution as sampling was conducted at only one site. The Lessepsianrabbitfish S. luridus was the only alien species we encounteredduring our visual fish surveys. S. luridus accounted for 37% ofherbivorous fish biomass and 6% of the total fish biomass. In mostcases, carnivores accounted for the largest proportion of totalbiomass, whereas apex predators represented a very smallproportion and were totally absent in some cases (island Strogylo).Fish trophic groups increased with total fish biomass across sites,except for apex predators (Table 1). Furthermore, carnivores werepositively correlated to herbivores and zooplanktivores.

On most islands, the dominant benthic group was turf algae(Fig. 2b). However, in Irakleia, Schinousa, Makares, Kato Koufo-nisi, Keros and Thirasia (all islands situated in the eastern part ofour study area) around 50% of the substrate was barren (barerock with calcareous algae), while in Kimolos, Strogylo andDonousa the dominant group was Cystoseira spp. The species ofthe genus Cystoseira identified in the study area includeC. barbata, Cystoseira spinosa, C. elegans, Cystoseira crinita,C. brachycarpa, C. foeniculacea, C. compressa, C. compressa var.pustulata and C. corniculata. Overall, the alien species coverage(98% corresponded to Caulerpa racemosa) accounted for a verysmall percentage with a mean value of 0.86% (st. dev. ¼ 1.86).There was no clear relationship between fish biomass and thestructure of benthic communities.

The total biomass for sea urchins ranged from 0 to 408.49 g m�2

whereas the average value across all sites was 63.74 gm�2. At islandlevel, biomass ranged from 0 to 164.83 g m�2 with a mean value of68.25 g m�2 (Fig. 2c). Overall, P. lividus presented higher biomassthan A. lixula, with mean value 36.94 g m�2 (st. dev.¼ 50.22) acrosssites, and 40.40 g m�2 (st. dev. ¼ 34.78) across islands. Therespective values for A. lixula were 26.79 g m�2 (st. dev. ¼ 46.82)and 28.22 g m�2 (st. dev. ¼ 23.73). In most islands size-frequencydistribution of sea urchins was unimodal with the mode repre-sented by individuals of 3e4 or 4e5 cm size (Appendix: Fig. A). Inthe islands: Serifos, Sifnos, Milos, Kimolos, Sikinos, Paros, Santoriniand Thirasia (most of them situated on the western part of thestudy area), the size-frequency distribution of the sea urchins wasbimodal with the first mode corresponding to 0e1 cm size indi-viduals and the second to 3e4 cm size individuals.

There was no significant relationship between total fish biomassand sea urchin biomass across sites (Table 1). Moreover, we did not

Fig. 2. a) Distribution of mean fish biomass among trophic groups (AP: apex predators, CA: carnivores, HE: herbivores, ZP: zooplanktivores), b) mean percentage coverage ofbenthos categories: ALIEN: alien species (Caulelrpa racemosa, Stypopodium schimperi and Asparagopsis taxiformis), CYM.NOD: Cymodocea nodosa, CAU.PRO: Caulerpa prolifera, TURF:turf algae, FAUNA: macroinvertebrates, SAR.SPP.: Sargassum spp., SAND, POS.OCE.: Posidonia oceanica, PEBBLES, DIC.SPP.: Dictyotales spp., CYS.SPP.: Cystoseira spp., CCA: crustosecoralline algae and BARE ROCK c) mean sea urchin (Paracentrotus lividus and Arbacia lixula) biomass. Values were estimated per island, where: SAN:Santorini, SER:Serifos,ANA:Anafi, PAR:Paros, THI:Thirasia, KIM:Kimolos, DES:Despotiko, SIK: Sikinos, FOL:Folegandros, ANT:Antimilos, IOS:Ios, MIL:Milos, KER:Keros, SIF:Sifnos, AMO:Amorgos, AKO: AnoKoufonisi, ANM: Antimilos, HRA:Irakleia, NAX:Naxos, SCH:Schinousa, DON:Donousa, POL:Polyaigos, KKO:Kato Koufonisi, MAK:Makares, STR:Strogylo.

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e104

find any significant relationship between sea urchins and carni-vores or Diplodus spp. (i.e. Diplodus sargus and Diplodus vulgaris)biomass (rs ¼ �0.064, p ¼ 0.39), which are the main predators ofadult sea urchins. Regarding the relationships between herbivoresand algal groups, we found that sea urchin biomass was positivelycorrelated with barren substrates and negatively correlated with

Table 1Spearman correlation values for fish trophic groups and sea urchins.

Zoo planktivores Herbivores

Zoo planktivores e �0.143 (p ¼ 0.60)Herbivores �0.143 (p ¼ 0.60) e

Carnivores 0.169* 0.288**Apex predators �0.082 (p ¼ 0.27) 0.015 (p ¼ 0.82)Total fish 0.525** 0.518**

** correlation is significant at p < 0.01,* correlation is significant at p < 0.05.

Dictyotales and turf algae (Table 2). S. cretense also displayeda negative relation to turf algae. The alien rabbitfish S. luridus wascorrelated negatively with the native canopy-forming algae Cys-toseira spp. and positively with P. pavonica.

The MDS analysis for sites and islands showed similarpatterns, therefore we only present the MDS for islands as it

Carnivores Apex predators Sea urchins

0.169* �0.082 (p ¼ 0.27) 0.525**0.288** 0.015 (p ¼ 0.82) 0.518**e 0.037 (p ¼ 0.62) 0.744**0.037 (p ¼ 0.62) e 0.117 (p ¼ 0.12)0.744** 0.117 (p ¼ 0.12) e

Table 2Spearman correlations among herbivores and major algal groups.

Sea urchins Sarpa salpa Sparisoma cretense Siganus luridus

Barren 0.574** 0.018 (p ¼ 0.81) 0.135 (p ¼ 0.69) 0.073 (p ¼ 0.33)Cystoseira spp. �0.102 (p ¼ 0.17) �0.090 (p ¼ 0.79) 0.076 (p ¼ 0.31) �0.171*Dictyotales �0.169* 0.053 (p ¼ 0.48) 0.062 (p ¼ 0.41) �0.027 (p ¼ 0.72)Padina pavonica �0.067 (p ¼ 0.37) 0.019 (p ¼ 0.80) 0.068 (p ¼ 0.36) 0.244**Turf �0.415** 0.023 (p ¼ 0.76) �0.183* 0.087 (p ¼ 0.24)

** correlation is significant at p < 0.01, * correlation is significant at p < 0.05.

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e10 5

provides clearer patterns (Fig. 3). The MDS for all sites showshigh dissimilarity between sites characterized by bare rock andthose with a canopy of Cystoseira spp., as well as between sitesthat were dominated by turf algae and those with large seaurchin biomass. The cluster analysis indicated 18 groups ofsamples, based on SIMPROF tests and according to the relativeabundance of the dominant groups. Cystoseira spp. and bare rockappeared as the two ends of a major axis, while turf algae andlarge sea urchin biomass the two ends of the other major axis.When MDS analysis was performed at the scale of island, clearerpatterns arose and therefore are graphically represented (Fig. 3).Five separate groups of islands were differentiated in the SIM-PROF analysis (Fig. 3). SIMPER analysis revealed that groupsdetermined by the SIMPROF test were characterized by thepresence of the same benthic category but differed from eachother by the relative abundance of the accompanying species.There was a clear association between sea urchins and barrens,opposed to abundant Cystoseira spp. and turf algae, and apexpredators; orthogonal to these two were other algal groups, andcarnivorous and herbivorous fish.

A significant variability at both spatial levels (island and site)was detected (Table 3). PERMANOVA indicated that greatestcomponent of variation occurred at the smallest spatial scale (i.e.replicates), followed by sites and lastly islands.

Fig. 3. MDS on fish trophic groups biomass, sea urchin biomass and algae cover f

4. Discussion

This is the first large-scale quantitative survey in the shallowsublittoral of the Cyclades Archipelago, North-eastern Mediterra-nean. Overall, a very low fish biomass was recorded compared toother areas in the Mediterranean Sea and no signs of trophiccascades were detected. The low abundance and biomass of seaurchins predators prevents them from controlling sea urchin pop-ulations. However, we found a gradient of canopy algae coverage,which may be affected by sea urchin grazing. There was a remark-able 83-fold range in fish biomass across islands, with valuesranging from 0.06 to 0.56 kg 125 m�2. It is of note that the highestfish biomass was found in the coastal waters surrounding Santorini,one of the most touristic islands of the Cyclades, with a compara-tively large fishing fleet. The lowest biomass was found in theuninhabited Strogylo, which is very close to Paros, the island withthe largest fishing fleet in the Cyclades. However, we surveyed onlyone site at Strogylo, due to its small size. Overall, the CycladesArchipelago had very low biomass values compared to fished areasnear protected areas in the Western Mediterranean. In those areas,fish biomass was at least 5 times higher with values ranging from2.3 kg 125 m�2, in Medes, to 5.3 kg 125 m�2, in Tabarca (García-Rubies and Zabala, 1990; Harmelin-Vivien et al., 2008; Garcia-Rubies, personal communication). The respective biomass values

or all islands. Five different groups were identified by the SIMPROF analysis.

Table 3PERMANOVA analyses based on BrayeCurtis dissimilarity for benthic data.VC ¼ Variance Components; BC diss. ¼ BrayeCurtis dissimilarity.

Source df Pseudo-F P (perm) VC BC diss (%)

Island 22 5.197 0.0001 494.61 22.24Site (Island) 146 7.015 0.0001 706.65 27.58Res 1495 1155.2 33.98Total 1663

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found inside the marine protected areas were 17.5 kg 125 m�2, inMedes, and 9.4 kg 125 m�2, in Tabarca. The most likely explanationfor the low fish biomass found in the Cyclades is historical overf-ishing combined to non-compliance of fisheries regulations,although other factors such as the extreme oligotrophy of theirwaters can also contribute to the low biomass maximum in theregion.

The study region has been subjected to human exploitationsince antiquity (Juanes, 2001). By Homer’s time (800e900 B.C.),fishing tools such as fine and pointed curved hooks (made ofmetal, bronze and iron), harpoons, nets of mesh sizes of 5e45 mmmade of hemp and flax were already present (Sahrhage andLundbeck, 1992). In the past century, the technological improve-ments in vessel construction, fishing gears and electronic devices(e.g. radars) in combination with large-scale non-selective gears(e.g. trawls) and the subsidy-driven overgrowth of the fishingsector has led to the unsustainable exploitation of marineresources (Stergiou, 2002). The estimates of fish stocks in Greekwaters are limited, due to scarcity of data and their limitedspatial distribution (SoHelFi, 2007). Yet, evidence shows thatdemersal and inshore marine resources are seriously over-exploited (Stergiou et al., 1997).

A variety of traditional management tools (e.g. maximummeshsize) have been incorporated into Greek fisheries regulations, toensure the sustainable use of marine resources. Furthermore, inGreek coastal waters trawling is prohibited within 1.5 nauticalmiles from the coast (or in waters shallower than 50 m), andpurse-seining is prohibited within 300 m from the coast (or inwaters shallower than 30 m). However, the virtual lack ofenforcement results in fishers often entering closed zones(SoHelFi, 2007), not respecting restrictions on fishing gears andusing dynamite, a non-selective and illegal fishing practise(Giakoumi unpublished observations).

An alternative hypothesis for the low fish biomass is the lowproductivity of the study region (SoHelME, 2005). However, webelieve this alone cannot explain the low fish biomass found at thestudy sites, given that the CabreraNational Park for example, an areaof similar productivity values (Coll et al., 2010), has biomass values24 times greater than the Cyclades (Harmelin-Vivien et al., 2008).Cabrera is a protected areawherefish biomass has increased relativeto the unprotected coast nearby, suggesting that, in the absence offishing, fish biomass at the Cyclades would also increase.

A factor that should be considered, regarding the low biomassrecorded, is the shallow depths where our study has been per-formed. Evidence shows that demersal fish species in infralittoralhabitats tend to increase in size along with depth (e.g. Macphersonand Duarte, 1991). In the Western Mediterranean, large specimensappeared to be more abundant at depths greater than 3 m (Tunesiet al., 2006). In our study, the apex predators were representedmainly by juvenile individuals and therefore their biomass asa group may have been underestimated. However, at shallowdepths, fish biomass displays much greater values in Mediterra-nean protected areas than in unprotected areas (Sala and Balles-teros, personal observations), which suggests that depth alone isnot the major cause of low apex predator biomass.

All fish functional groups increased in biomass as total biomassincreased, except for apex predators. Although a very lowpercentage of total biomass corresponded to apex predators,which is typical in Mediterranean fishing grounds (Macphersonet al., 2002), there was no significant correlation between apexpredators’ and total fish biomass. It is important that apex pred-ators were recorded only in 44 out of 181 sites, which indicatesa depleted ecosystem. Only in pristine areas and well-enforcedmarine reserves, with large fish biomass, there is an increase intotal fish biomass accompanied by larger increase in apex preda-tors’ biomass than in other functional groups (Newman et al.,2006; Sandin et al., 2008). In such pristine habitats, top preda-tors correspond to the largest proportion of total fish biomass,presenting an inverted (top-heavy) biomass pyramid (DeMartiniet al., 2008; Sandin et al., 2008).

In the Cyclades Archipelago, we found lower abundance ofpredatory fish than in the Central and Western Mediterranean(Guidetti and Dul�ci�c, 2007; Guidetti and Sala, 2007; Harmelin-Vivien et al., 2008). The lack of a significant relationshipbetween predatory fish and sea urchins was expected in islandswith such low Diplodus numbers, which are the main predatorsof adult sea urchins (Sala, 1997a). Guidetti and Sala (2007) founda critical threshold for Diplodus spp. (15 adult ind. 100 m�2)above which predation exerts top-down control of sea urchinpopulations. The sparids’ density recorded throughout the studyarea was much lower than that threshold. Thus, Diplodus spp.appear not to be able to control sea urchin populations in theCyclades. Nevertheless, the average total biomass of P. lividus andA. lixula found was also low compared to some Mediterraneanareas such as southern and northern Italy (Guidetti et al., 2003;Micheli et al., 2005; Chiantore et al., 2008) but similar tovalues reported from other Mediterranean islands such asMinorca (Cardona et al., 2007) or Sardinia (Guidetti et al., 2004).The fact that in some islands the size-frequency distribution ofsea urchins was bimodal, while in others it was unimodal, cannotbe attributed to differences in predation rates. The density andbiomass of sea urchin predators was very low in the entire studyarea. One possible explanation could be the differences in vege-tation coverage. In the islands where most sites were barren ordominated by turf algae we did not record many small individ-uals. Those individuals may have been hidden in crevices orunder boulders (to escape predation). Consequently, the esti-mation of their abundance may have been underestimated.Availability of shelter, diseases, pollution, temperature, waveexposure and sea urchin harvesting are other factors that mayregulate Mediterranean sea urchin populations (Sala et al., 1998;Hereu et al., 2004). In the Cyclades, harvesting cannot beconsidered as a controlling force for sea urchin abundance asthey are not commercially exploited.

We observed a gradient of benthic community complexity fromsea urchin barrens to communities dominated by canopies of thebrown algae Cystoseira. Barrens were spread all over the studyarea, whereas sites with high cover of Cystoseira spp., interestinglywere situated in north-northwestern locations. This variability inthe abundance of Cystoseira stands related to orientation has alsobeen found in other studies (Sales and Ballesteros, 2009). North-oriented locations are affected by strong northern winds (partic-ularly during summer) that hinder urban development, thushelping to preserve coastal environments although greater watermovements in the northern coasts could also explain this pattern.This is also a gradient of benthic biomass, since Cystoseira spp.account for most of the biomass and production of the shallowrocky algal assemblages (Ros et al., 1985; Ballesteros, 1989).Associated with the benthic biomass gradient there is alsoa biodiversity gradient, since Cystoseira assemblages harbour

Table BFish species and families identified by visual census in the 181 sites with hardsubstrate and their assignment in trophic groups. ZP: zooplanktivores, HE: herbi-vores, CA: carnivores, AP: apex predators.

Family e Species Trophicgroup

Family e Species Trophicgroup

Apogonidae Serranus scriba CAApogon imberbis CA LabridaeAtherinidae ZP Labrus bergylta CABlenniidae CA Labrus merula CASparidae Labrus viridis CABoops boops ZP Symphodus cinereus CADentex dentex AP Symphodus doderleini CADiplodus annularis CA Symphodus mediterraneus CADiplodus puntazzo CA Symphudus melanocercus CAD. sargus CA Symphodus ocellatus CA

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e10 7

a high biodiversity (e.g. Boudouresque, 1972; Ballesteros et al.,1998, 2009). Furthermore, the diversity and biomass of benthicinvertebrates also increases with an increase in algal biomass(Sala, 1997b). In the Mediterranean, the sea urchins P. lividus and A.lixula are considered to be responsible for the decrease in Cys-toseira coverage and the development and maintenance of barrens(Verlaque, 1984; Frantzis et al., 1988; Sala, 1997a; Bulleri et al.,1999).

The quantitative baseline provided by the present study isrequired for the future evaluation of changes in the region due tofishing, the introduction or increase in abundance of exotic species,or by potential management measures such as the identification ofareas where to prioritize the establishment of marine protectedareas (e.g. Giakoumi et al., 2011).

D. vulgaris CA Symphodus rostratus CAOblada melanura CA Symphodus roissali CAPagrus pagrus CA Symphodus tinca CAPagellus acarne CA Xyrichthys novacula CAS. salpa HE Thalassoma pavo CASpondyliosoma cantharus CA Coris julis CALithognathus mormyrus CA Mugilidae CAEngraulidae MullidaeEngraulis encrasicolus ZP Mullus surmuletus CACarangidae MuraenidaeSeriola dumerili AP Muraena helena APTrachinotus ovatus CA SciaenidaeTrachurus mediterraneus CA Sciaena umbra CACentracanthidae ScorpaenidaeSpicara maena ZP Scorpaena porcus CASpicara smaris ZP Scorpaena scrofa APGobiidae CA SiganidaePomacentridae S. luridus HEChromis chromis ZP Sphyraenidae

Acknowledgements

We would like to thank Dr. A. Garcia-Rubies for providing usunpublished data as well as two anonymous reviewers for theiruseful suggestions which improved significantly previousversions of the manuscript. Special thanks to M. Sini, A. Spyr-opoulou, A. Pantazis, I. Vlachou and A. Gómez for their invalu-able efforts during the underwater surveys. Funding for materialand field expenses was provided by the Prefecture of theCyclades. A Hellenic State Postgraduate Scholarship (IKY) wasawarded to S. Giakoumi. This is a contribution of GRACCIEproject (CSD2007-00067).

Serranidae Sphyraena sphyraena APEpinephelus costae AP ScaridaeEpinephelus marginatus AP S. cretense HEMycteroperca rubra AP Tripterygiidae CASerranus cabrilla CA

Appendix

Table AParameter values used for the lengtheweight relationship.

Family/Species a b Family/Species a b

Apogon imberbis 0.0124 3.108 Serranus cabrilla 0.0277 2.725Atherinidae 0.0077 3.029 Serranus scriba 0.0095 3.122Blenniidae 0.0109 3.025 Labrus bergylta 0.0119 3.115Boops boops 0.0149 3.093 Labrus merula 0.0105 3.076Dentex dentex 0.0147 2.966 Labrus viridis 0.0359 2.669Diplodus annularis 0.0231 3.002 Symphodus cinereus 0.0033 3.012Diplodus puntazzo 0.0044 2.662 Symphodus

mediterraneus0.0144 3.012

Diplodus sargus 0.0138 3.070 Symphudusmelanocercus

0.0180 3.000

Diplodus vulgaris 0.0131 3.055 Symphodus ocellatus 0.0083 3.221Oblada melanura 0.0219 2.831 Symphodus rostratus 0.0031 3.486Pagrus pagrus 0.0200 3.105 Symphodus roissali 0.0350 2.670Pagellus acarne 0.0150 2.933 Symphodus tinca 0.0278 2.733Sarpa salpa 0.0145 2.978 Xyrichthys novacula 0.1033 2.235Spondyliosoma

cantharus0.0339 2.849 Thalassoma pavo 0.0159 2.972

Lithognathusmormyrus

0.0110 3.196 Coris julis 0.0048 3.378

Engraulis encrasicolus 0.0013 3.590 Mugilidae 0.0130 2.955Seriola dumerili 0.0225 2.847 Mullus surmuletus 0.0140 2.954Trachinotus ovatus 0.0220 2.730 Muraena helena 0.0017 2.953Trachurus

mediterraneus0.0099 2.900 Sciaena umbra 0.0352 3.048

Spicara maena 0.0104 3.096 Scorpaena porcus 0.0236 2.887Spicara smaris 0.0069 3.247 Scorpaena scrofa 0.0169 2.999Gobiidae 0.0212 2.917 Siganus luridus 0.0110 3.040Chromis chromis 0.0996 2.415 Sphyraena sphyraena 0.0648 2.320Epinephelus costae 0.0024 3.440 Sparisoma cretense 0.0113 3.052Epinephelus

marginatus0.0127 3.085 Tripterygiidae 0.0066 3.125

Mycteroperca rubra 0.0166 3.000

Fig. A. Size-frequency distributions of sea urchins (test diameter without spines). The black part of the bar corresponds to Arbacia lixula and the grey to Paracentrotus lividus.

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e108

S. Giakoumi et al. / Estuarine, Coastal and Shelf Science 109 (2012) 1e10 9

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