Available online at www.sciencedirect.com

s 70 (2008) 182–195www.elsevier.com/locate/jmarsys

Journal of Marine System

Temporal trends of littoral fishes at deep Posidonia oceanicaseagrass meadows in a temperate coastal zone

Salud Deudero a,⁎, Gabriel Morey b, Antoni Frau a, Joan Moranta b, Isabel Moreno a

a Laboratorio de Biología Marina, Departamento de Biología, Guillem Colom, Campus Universitari,Ctra. de Valldemossa, km 7.5, 07122 Palma de Mallorca, Spain

b Institut Mediterrani d'Estudis Avançats-CSIC/UIB, Miquel Marques 21, 07195 Esporles, Spain

Received 20 December 2005; received in revised form 7 December 2006; accepted 1 May 2007Available online 16 May 2007

Abstract

Seasonal abundance and biomass of littoral fish at Posidonia oceanica seagrass meadows were characterized throughout anannual cycle in Mediterranean waters. Bimonthly beam trawl hauls were performed between 18 and 38 m depth at 4 sites samplingfrom 2 locations. Approximately 8230 littoral fish were collected belonging to 25 families and 51 species with Labridae andSparidae families being predominant in terms of abundance. Mean fish abundance was 92±7.5 individuals ·1000 m−2 peaking inMarch, April and September and total abundance showed significant statistical differences between May and October. Densities ofDiplodus annularis, Gobius sp., Mullus surmuletus, Parablennius tentacularis, Sarpa salpa, Sciaena umbra, Scorpaena porcus,Serranus cabrilla, Symphodus ocellatus, Symphodus rostratus, Symphodus tinca and Synodus saurus differed significantlybetween seasons. Total community biomass varied significantly along the year with maximum values observed in July (1500g ·1000 m−2) and minimum biomass recorded in October. The number of species ranged between 5 in January and 21 in July whilethe total number of individuals was 293 in July and 21 in September, and Margalef diversity index differed between 4.11 in Julyand 1.3 in January. Biomass peaked in summer linked mainly to the increase of S. porcus, Serranus scriba and some Symphodusspecies. Diversity was maximal in July and the larger mean size for most of the fish species was achieved from May to Julycorresponding to the recruitment peaks of some of the fish species. The SIMPER analysis showed that there are seasonaldifferences in the trophic roles of the fish communities at seagrass meadows. The temporal patterns observed highlight themultifunctional role of deep seagrass meadows during the summer months when all the measured parameters are maximal. Thoseobservations point out the need for conservation measures to be intensified in the warm season.© 2007 Elsevier B.V. All rights reserved.

Keywords: Fish seasonality; Posidonia oceanica; Community structure; Western Mediterranean; Balearics

1. Introduction

The important multifunctional role that seagrassesexert in contributing to the productivity of the coastalzone and in providing habitat and resources to inver-

⁎ Corresponding author. Tel.: +34 971173138; fax: +34 971173184.E-mail address: salud.deudero@uib.es (S. Deudero).

0924-7963/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.jmarsys.2007.05.001

tebrate and fish communities is well know in severalseas (Jackson et al., 2001; Tanner, 2005) In theMediterranean Sea, meadows of the endemic speciesPosidonia oceanica (L.) Delile constitute one of themost extensive littoral ecosystems, reaching about50,000 km2 (Bethoux and Copin-Montegut, 1986),and playing an important role both from their produc-tivity and structural functions, as well as a recruitment

183S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

area for many fish species (Proccacini et al., 2003). Themain population of P. oceanica is located in the BalearicIslands, where it occupies nearly 2000 km2 constituting70% of the Spanish coastal meadows (Mas et al., 1993).Although P. oceanica meadows are considered as theclimax community over infralittoral sandy bottoms, theyare subjected to a recession process (Marbà and Duarte,1997), and their community structure as well as thepopulation dynamics, have been widely used fordetecting human-related changes (Short and Wyllie-Echevarria, 1996; Guidetti and Fabiano, 2000). Simi-larly, the associated fauna can be used for determiningthe conservation status of these ecosystems (Guidettiand Bussoti, 2002). At a meso-scale level, fishassemblages are considered as a good indicator of thecondition of the P. oceanica meadows, because manyspecies are resident and show high site fidelity (Bell andHarmelin-Vivien, 1982; Sanchez-Jerez and Ramos-Espla, 1996).

Sampling of fish assemblages for seagrass meadowshas been carried out worldwide using several methods,such as poisoning (Bell and Westoby, 1986), seining(Howard, 1987; Guest et al., 2003), visual censuses(Harmelin-Vivien et al., 1985; Sanchez-Jerez andRamos-Espla, 1996; Francour, 1997) and small trawlnetting (Bell and Harmelin-Vivien, 1982, 1983;Reñones et al., 1995). Most of the P. oceanica meadowsare found at depths that do not allow using seine nets,rotenone present secondary effects together with theneed of sampling a large area, visual censuses quantifyonly species occurring above the meadow (e.g.,planktivores) and the largest and fast-swimming species.Conversely, beam trawl is known to record moreefficiently benthic and cryptic species (Harmelin-Vivienand Francour, 1992), thus resulting in a precise approachto the fish assemblage characterization (Lipej et al.,2003). Therefore, beam trawl is adequate for detectingspatial and temporal variations (Petrik and Levin, 2000)and it was preferred for sampling the fish faunaassociated to P. oceanica meadows because it allowsto sample larger areas, catch more individuals andspecies, specially those more abundant in the meadow(e.g., Serranus scriba, Symphodus ocellatus, Sympho-dus rostratus).

Several studies have dealt with spatial or dielvariation of fish fauna (Valle et al., 2001; Guest et al.,2003; Hyndes et al., 2003). At the Western Mediterra-nean, studies on patterns of spatial variation of the P.oceanica seagrass beds fish assemblage have mainlyfocussed on comparative analyses inside and outsidemarine protected areas (e.g., Francour, 1994, 1997;Macpherson et al., 2002) or on the impact of bottom

trawling (Sanchez-Jerez and Ramos-Espla, 1996; Jime-nez et al., 1997). Similarly, temporal trends atpluriannual level have been studied associated to thereserve effect (Francour, 1994, 1997). Nevertheless, inthe Balearic Islands the associated fish fauna has onlybeen described from a single locality (Massutí, 1965;Reñones et al., 1995), but no studies have focussed onthe temporal variability in fish composition, abundanceand biomass at deep seagrass meadows in theMediterranean. Other studies have applied to beamtrawl as a methodological approach to study the fishfauna at seagrass beds (Ferrell et al., 1993; Guest et al.,2003; Hyndes et al., 2003) and some address the effectsof trawling on fishes associated to P. oceanica meadows(Guillen et al., 1994; Sanchez-Jerez and Ramos-Espla,2000).

The objective of this study was to analyse the effectof seasonality on the littoral fish community associatedto deep seagrass beds along a one-year cycle at differentlocalities from temperate waters.

2. Materials and methods

2.1. Description of study site

Two localities, Camp de Mar (39°31′N, 2°24′E) andMalgrats (39°30′N, 2°27′E), 3.32 nautical miles apart,were selected in the south-western coast of MallorcaIsland (Balearics, NW Mediterranean). Two samplingsites, hundreds of meters apart each other, wereestablished within each locality. Sites were maintainedthrough all the surveys, and three tows were randomlycarried out within each site during each survey,totalising 96 samples.

2.2. Field sampling and data analysis

The fish community was sampled bimonthly betweenMay 2002 and March 2003, over P. oceanica beds atdepths ranging from 11 to 38 m (mean 22±5.8 SD),using a beam trawl during daytime (10:00–13:00 h). Thebeam trawl was 1.8 m wide and 0.8 m high, with a bodyof 8 m (12 mm square mesh at its first half and 9 mm atthe back), and a 2 m long cod end (6 mm square mesh).Each beam trawl was towed, whenever possible, during15 min at a mean speed of 1.5 knots. All fishes wereidentified, counted, measured (to the lowest mm) andweighed (to the lowest 0.01 g) at the laboratory.Abundances and biomasses were standardized to1000 m2, and the results were referred to this area.

Length–frequency analysis (LFA) on the mostabundant fish species Coris julis, Diplodus annularis,

184 S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

Scorpaena porcus, S. ocellatus, S. rostratus, S. scribawere performed with a Kolmogorov–Smirnov test(STATISTICA 6.0). For each species, data from eachsingle survey were pooled allowing LFA comparisonsbetween months, but excluding comparisons betweenlocalities.

Biomass spectra (Platt and Denman, 1978) of themain fish species were calculated for each location andmonth. Fishes larger than 1 g were assigned to log2 bodymass class in grams, and cumulative biomass in eachbody mass class was calculated. Normalized biomasssize spectra were computed dividing the biomass in agiven body mass class interval by the width of that classinterval (in antilog dimensions). The relationshipbetween normalized biomass and class interval wasestimated using least squares regressions (Macphersonand Gordoa, 1996). The regressions were performedseparately for each location and were compared bymeans of Analysis of Covariance. Values to the left ofthe mode in the distribution of biomass by size intervalwere subsequently excluded from the regressionanalysis as they did not contribute to slope determina-tion. A slope equal to −1 indicates an even distributionof biomass over the size spectra; a slope steeper than −1indicates a decrease in biomass with size, and a slopeflatter than −1 indicates an increase in biomass withsize.

Multivariate statistics (PRIMER software package v5.0, Clarke and Gorley, 2001) was applied to testchanges in community structure. Data were fourth roottransformed and a Bray–Curtis similarity coefficientwas calculated. The SIMPER routine was performed onfish abundance data in order to evaluate the average

Fig. 1. Mean abundance of fish species representing 90% of the total fish aMalgrats location. Error bars stand for standard error.

percentage of intra-group similarity (i.e., within eachsampling season) and the average percentage of inter-group similarity (i.e., between sampling seasons). Thisprocess also allowed for an assessment of which speciescontributed to either the similarity within or dissim-ilarity among the grouped data (Clarke and Warwick,1994).

Trophic characteristics of the fish assemblages wereassessed by grouping the fish species into feeding guildsin agreement with previous studies by Deudero et al.(2004) and Malavasi et al. (2004): strictly invertebratefeeders (IS), invertebrate feeders/fish feeders (IF),carnivorous feeders (CS), strictly fish feeders (FS),herbivorous/carnivorous feeders (HC), herbivore strict(HF), strictly planktivorous feeders (PS). A SIMPERanalysis (PRIMER, v5) was calculated on the averagecontribution of the fish feeding guilds to test theexistence of seasonal differences in the trophic roles ofthe fishes involved in the seagrass meadows.

A three-way ANOVAwas applied to determine if theabundances of each fish species differed betweenmonths, locations and sites. All factors were consideredto be fixed. The sampling design was set as follows:months (T) with eight treatments corresponding to theeight sampling times; location (L) with two locations atCamp de Mar and Malgrats and with an interaction withmonths; and site (S) with two treatments correspondingto the two sampling sites, being a nested factor with theinteraction of T and L. In all cases, data were log (x+1)transformed since Levene test demonstrated heterosce-dastic data. Tukey test, which corrects for multiplecomparisons, was used to determine significant differ-ences among means in the case of interactions.

bundance. Black bars represent Camp de Mar location and white bars

185S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

The influence of the multivariate descriptors (loca-tion, depth, season and month) over the speciesabundances was analysed using redundancy analysis(RDA). RDA allows testing hypotheses properly in thecase of hierarchically nested sampling designs usingpermutation-based tests (split-plot design routine inCANOCO 4.5; ter Braak and Smilauer, 2002). Toanalyse the effect of seasonality, the sampling monthswere grouped in two seasons, warm (July, September,October) and cold (January, March, May, April andDecember). In addition to testing the variabilityexplained at different sampling scales it is also possibleto test the effects of specific environmental variables.Only those species appearing in more than 5 hauls andwith a total abundance higher than 0.5% were includedin the analysis.

3. Results

Depth ranged between 15 and rather than 25 m atthe two studied locations. The seabottom was char-acterized by P. oceanica seagrass beds with mediumsand and gravel sediment grain size. Temperatureranged from 14.1 °C in March to 25.7 °C inSeptember, with a thermal range of 10 °C. The esta-blishment of the thermocline was observed from Mayto September.

3.1. Species composition and seasonality in abundanceand biomass

Approximately 8230 littoral fish were collected overthe study period corresponding to 25 families and 51species. Dominant families included labrids (S. rostra-tus, C. julis, S. ocellatus, Symphodus mediterraneus),sparids (D. annularis, Diplodus vulgaris), serranids (S.scriba) and scorpaenids (S. porcus) (Table 1). Labridaespecies represented 51% of the total abundance, whileSparidae stand for 18% and Serranidae for 15%followed by Pomacentridae (7%), Scorpaenidae (4%)and Gobidae (2%).

In terms of biomass S. scriba represented 19.3%, S.porcus 18.7%, S. rostratus 11.3%, D. annularis 9.8%,C. julis 7.6%, Chromis chromis 7%, S. ocellatus 4.7%,Symphodus tinca 4% and Scorpaena scrofa 2.3% ofthe total community biomass throughout the year.

Seasonality in species composition is clearly envi-saged in terms of abundance. Eight fish speciesrepresented 95% of the total abundance being S.rostratus, D. annularis, C. julis, S. ocellatus, S. scriba,S. porcus, S. mediterraneus and Gobius cruentatus.Mean density was 92±7.5 individuals ·1000 m−2 peak-

ing in March, April and September (Fig. 2). Location 2(Camp de Mar) exhibited higher densities than location1 (Malgrats), especially in September and April. Totalabundance (log x+1) showed an interaction betweenTime and Location and an interaction between sitenested in the interaction of Time and Location (three-way ANOVA, pb0.005) with significant statisticaldifferences in abundances between May and October(Tukey test) (Fig. 1).

The occurrence of the syngnathid species Syng-nathus acus, Syngnathus typhle and Nerophis maculatuswas observed throughout the year, especially those of S.typhle. Densities of these pipefishes were rather low(Table 1) and size ranges corresponded to juvenile andadult specimens.

Maximum biomass was observed in July with valuesof 1500 g ·1000 m−2 (Fig. 2). Minimum biomass valueswere recorded in October with 500g ·1000 m−2. Totalbiomass varied significantly during the year and wasinfluenced by an interaction between Site nested in theinteraction of Time and Location (three-way ANOVA,pb0.005). Significant differences in total biomasswere found among January, July, October and December(Tukey test).

3.2. Seasonal effects on fish assemblages

Densities of D. annularis, Gobius sp., Mullussurmuletus, Parablennius tentacularis, Sarpa salpa,Sciaena umbra, S. porcus, Serranus cabrilla, S.ocellatus, S. rostratus, S. tinca and Synodus saurusdiffered significantly among seasons (ANOVA, Table2). The effect of Location was observed in D. vulgaris,Gobius sp., S. salpa, S. porcus, S. scriba, Spondylio-soma cantharus, Symphodus cinereus, S. tinca, S. typhleand S. saurus. A Time/Location interaction was foundfor Gobius sp., P. tentacularis, S. umbra, S. cabrillaand S. saurus. The mean density of D. vulgaris, C. julis,Gobius sp., P. tentacularis, S. umbra, S. tinca and S.saurus was significantly affected by the sampling Sitethat was nested in the interaction of Time/Location(Table 2).

SIMPER analysis showed that the most representedspecies in terms of percentage contribution to theaverage abundance along the year were S. scriba, S.cabrilla, S. rostratus, S. ocellatus, S. mediterraneus, D.annularis, C. julis, S. porcus and G. cruentatus (Fig. 3).There are seasonal differences in the average abundanceof each fish species. For example, C. julis exhibitsmaximum contribution to the total abundance in Apriland minimum in October, similar patterns are observedfor D. annularis.

Table 1

Overall seasonal catches of fishes at seagrass beds

Species May 2002 July 2002 September 2002 October 2002 December 2002 January 2003 March 2003 April 2003

Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE Size x̄ ±SE

Apletodon dentatus 3–3 0.11±0.15

Apogon imberbis 8.6–8.6 0.11±0.15

Bothus podas 9.5–11.1 0.21±0.20 5.5–12 0.43±0.34 5.7–5.7 0.11±0.15 7.5–9 0.21±0.30 13.5–13.5 0.11±0.15 7.5–9.5 0.21±0.30 9.5–11.5 0.21±0.30

Coris julis 5.7–10.5 4.61±2.86 5.5–13 52.71±32.90 3.2–13.6 4.29±1.77 4–14.5 0.96±0.68 4–12.6 1.07±0.67 5–12.5 0.43±0.34 3.5–12.5 0.59±0.26 4–12 0.70±0.47

Chromis chromis 6.2–10.4 15.64±4.81 5–11 14.78±3.98 3.2–10.1 12.86±3.72 4.5–8.4 9.53±3.08 4.5–9 22.28±4.40 5.3–7.7 12.96±4.01 5.5–9.5 21.37±8.36 5.5–9.5 24.69±8.85

Dactylopterus volitans 27.5–27.5 0.11±0.15

Diplodus annularis 5–14 18.75±6.30 2–15 14.46±2.39 3–15.7 24.86±6.69 4.2–14.2 17.14±2.82 4–8.5 9.96±3.44 4.2–11.5 12.64±2.77 4–14 22.87±5.44 4.5–16.5 24.11±5.68

Diplodus puntazzo

Diplodus vulgaris 8.7–13.2 3.00±1.27 6–13 2.04±0.85 7.5–14.1 0.96±0.40 4.3–10.2 0.96±1.21 9.5–9.5 0.11±0.15 9–13.8 0.75±0.65 10–10 0.11±0.15 8.5–12.5 0.91±0.51

Gobius cruentatus 7.8–15.2 1.39±0.99 8.5–17 0.96±0.33 5.5–12.3 1.18±0.61 6.7–12 1.50±0.59 6.5–14 1.82±0.91 5.8–13.4 1.50±0.74 6.5–13 2.25±0.68 6.5–13 2.30±1.09

Gobius falax 19.2–19.2 1.27±1.02 10–15 1.87±1.64 5–5.3 0.21±0.30 6.3–7.3 0.32±0.33

Gobius paganellus 7.2–7.2 0.11±0.15 9–9 0.11±0.15

Gobius sp. 5.5–6.5 0.21±0.20 13–14

Gobius buchichi 6.5–6.5 0.11±0.15

Labrus merula 29.5–29.5 0.11±0.15

Labrus viridis 22.4–29 0.21±0.20 37.5–39.5 0.21±0.30 26–26 0.11±0.15 30–30 0.11±0.15 26.1–26.1 0.11±0.15

Lepadogaster lepadogaster 2.1–2.1 0.11±0.15

Mullus surmuletus 6.5–8.5 5.25±2.44 7.2–11.9 1.29±0.63 10.3–14 0.43±0.34 11–14.3 0.21±0.20 14–23.3 0.21±0.30

Muraena helena 70–70 0.11±0.15

Nerophys maculatus 23–23.4 0.21±0.20 20–20 0.11±0.15 24–24.5 0.21±0.30 23.3–24 0.21±0.30 22–22 0.11±0.15

Pagellus spp 5–7.5 0.21±0.20

Parablennius tentacularis 7.6–9.5 0.43±0.41 9–9 0.11±0.15 6.4–8.6 0.64±0.61 8.3–8.3 0.11±0.15 6.5–11 0.56

Parophidion vassali 16.5–16.5 0.11±0.15 11.8–14.7 0.21±0.20 8.7–8.7 0.39±0.45 4.7–9.5 0.45±0.23

Raja radiatus 27–27 0.11±0.15

Sarpa salpa 15.5–19 0.54±0.35 14.1–14.4 0.32±0.24 14.5–15.4 0.21±0.20 22–22 0.16±0.16

186S.

Deudero

etal.

/Journal

ofMarine

Systems70

(2008)182–195

Sciaena umbra 9–10 0.52±0.50 13–13 0.1±10.15 25–25 0.21±0.20

Scorpaena notata 7.6–11.7 0.75±0.76 5.7–8.9 0.32±0.33 7–8.6 0.32±0.33 7.5–9.5 0.43±0.34 8–10.4 0.32±0.24 3.6–9.2 0.64±0.27 6–11 0.59±0.47

Scorpaena porcus 9.4–22.5 2.25±1.17 11.5–26 3.43±1.29 6–23.5 5.25±1.65 7.9–21.8 2.46±0.96 3.5–23.4 3.54±1.21 6.8–22.2 3.21±1.13 6.5–24 6.21±1.48 6.5–22.5 3.59±1.05

Scorpaena scrofa ± 19–19 0.11±0.15 14.3–16 0.21±0.20 14.1–23 0.32±0.33 10.5–22.2 0.43±0.26 11–33 0.21±0.20 7.3–20.5 0.21±0.20 25–25 0.11±0.15

Serranus cabrilla 7.1–10 0.54±0.35 11–12 0.21±0.20 4.6–11.7 2.79±1.24 4.3–8.6 1.50±0.80 6.5–9.5 2.68±0.88 6.6–9.6 1.82±0.69 6–10.5 1.77±1.16 5.5–10.5 1.34±0.60

Serranus hepatus ± 7–7 0.11±0.15 ± 5.7–5.7 0.11±0.15 5.7–5.7 0.11±0.15 5.5–5.5 0.11±0.15

Serranus scriba 5.3–19.7 11.46±3.75 7.5–7.521 14.36±3.58 5.8–16.6 18.53±4.91 5–16.3 15.43±3.85 5–19.4 11.25±3.66 4.3–18 12.00±3.64 5–21 14.95±4.05 5.5–18.5 18.32±4.05

Solea sp. 5.3–8.4 0.11±0.15 6.8–6.8

Spicara smaris 10.8–13.6 1.50±1.96 13–14.5 0.32±0.45

Spondyliosoma cantharus 15.5–15.5 0.11±0.15 7.5–16.5 0.75±0.42 10.6–10.6 0.11±0.15 9–9 0.11±0.15

Symphodus cinereus 6.7–10.2 1.71±0.85 7–8 0.54±0.35 3.9–9.5 1.07±0.74 3.8–8.7 0.54±0.35 4–8.5 1.39±0.82 4.7–8.4 1.71±1.17 4.5–8.6 1.71±0.82 5.5–9.5 0.86±0.65

Symphodus doderleini 9.5–9.6 0.21±0.20 4–9.5 0.43±0.26 6–10.1 0.86±0.41 6.6–6.6 0.11±0.15 4–9.6 0.75±0.35 7.3–11.7 0.43±0.34 7.5–10 0.91±0.39 7–10 0.96±0.40

Symphodus mediterraneus 5–13.7 2.68±0.91 2.5–11.5 2.46±1.11 3.6–40.5 3.21±1.28 4.7–12.6 1.18±0.76 4–14.8 2.36±0.74 4.1–10 2.14±0.98 2.2–11 2.89±0.68 5–12 4.50±1.33

Symphodus melanocercus 8–8 0.11±0.15

Symphodus ocellatus 1.9–10.5 23.03±5.12 4–10 16.93±3.68 2.8–10.1 19.18±3.53 3–10.6 8.89±2.85 3–8.9 9.64±2.37 3.5–10.7 4.39±1.41 4–8 10.39±3.32 4.5–9 31.66±8.02

Symphodus roissali 11–11 0.11±0.15

Symphodus rostratus 6.7–10.6 11.68±2.20 3.5–11 13.93±2.74 4–11.1 21.00±5.86 5–12 10.50±2.38 5–10.5 20.68±3.96 4.4–11 22.82±3.84 5–11 29.89±3.27 5.5–11 18.16±3.26

Symphodus tinca 11.3–25.2 1.61±0.45 12–21.5 1.39±0.61 12.2–17.9 1.39±0.61 14.5–20.7 1.18±0.52 16–23 0.64±0.52 13–17 0.70±0.38

Syngnathus acus 26–26 0.11±0.15 22.2–22.7 0.32±0.33 20–20 0.11±0.15 25–27 0.37±0.24

Syngnathus typhle 19–29 0.75±0.42 16.2–25.5 1.71±0.79 14.5–23 0.64±0.35 11.7–26.5 1.29±0.55 16–29 1.50±0.70 10–27 0.86±0.41 12.3–27.5 1.29±0.39 30–40 0.32±0.33

Synodus saurus 8.2–8.2 16.5–16.5 0.11±0.15 12.5–12.5 0.11±0.15 6.5–24 0.70±0.52 8.5–24.5 0.54±0.35

Trachinus draco 7–10 0.21±0.20

Uranoscopus scaber 22–29.2 0.21±0.20

Zeus faber 20–20 0.11±0.15

Size= length range (cm); x̄ =mean abundance (ind·1000 m−2); SE=standard error.

187S.

Deudero

etal.

/Journal

ofMarine

Systems70

(2008)182–195

Fig. 2. Mean seasonal biomass for Camp de Mar (black bars) and Malgrats (white bars). Error bars stand for standard error.

188 S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

3.3. Seasonal changes in size distribution

The monthly mean length and size interval for someof the key fish species is shown in Fig. 4. S. ocellatusand S. rostratus presented maximum mean length inMay, while D. annularis, S. porcus and S. scriba werelarger in July. The rest of the species for which the

Table 2Results on the analysis of variance (three-way) of the abundance of fish spe

Species

D. vulgaris C. julis D.

Source of variation df MS MS MTime 7 0.296 0.223⁎ 0.Location 1 0.197⁎⁎⁎ 0.365 0.Time×Location 7 0.199 0.18 0.Site (Time×Location) 16 0.058⁎⁎ 0.203⁎ 0.Residual 64 0.055 0.102 0.

Species

S. salpa S. umbra S.

Source of variation df MS MS MTime 7 0.031⁎ 0.005⁎ 0.Location 1 0.112⁎⁎ 0.001 0.Time×Location 7 0.017 0.007⁎ 0.Site (Time×Location) 16 0.011 0.006⁎⁎ 0.Residual 64 0.01 0.002 0.

Species

S. cinereus S. ocellatus S.

Source of variation df MS MS MTime 7 0.071 0.872⁎⁎⁎ 0.Location 1 0.986⁎⁎⁎ 0.012 0.Time×Location 7 0.109 0.081 0.Site (Time×Location) 16 0.069 0.085 0.Residual 64 0.075 0.114 0.

MS, mean squares; p, level of probability; ⁎pb0.05; ⁎⁎pb0.01; ⁎⁎⁎pb0.00

length frequency distribution was analysed showedmaximum mean size in the May–July period, with theexception of C. julis with higher mean size in October.

The Kolmogorov–Smirnov test did not show cleartrends for the length frequency analysis of the six mostcommon species (C. julis, D. annularis, S. porcus, S.scriba, S. ocellatus and S. rostratus). The mean size of

cies

annularis Gobius sp. M. surmuletus P. tentacularis

S MS MS MS283⁎⁎ 0.005⁎ 0.494⁎⁎⁎ 0.05⁎

176 0.005⁎⁎⁎ 0.05 0.00113 0.005⁎ 0.065 0.047⁎

15 0.005⁎⁎⁎ 0.046 0.047⁎⁎

095 0.001⁎⁎⁎ 0.053 0.02

porcus S. cabrilla S. scriba S. cantharus

S MS MS MS23⁎ 0.242⁎⁎ 0.157 0.045698⁎ 0.103 2.918⁎⁎⁎ 0.005⁎⁎⁎

12 0.152⁎ 0.032 0.005099 0.08 0.176 0.015102 0.07 0.101 0.01

rostratus S. tinca S. typhle S. saurus

S MS MS MS283⁎⁎⁎ 0.241⁎⁎⁎ 0.096 0.048⁎⁎⁎

166 0.21⁎ 0.47⁎⁎ 0.077⁎⁎

053 0.044 0.108 0.041⁎⁎⁎

04 0.093⁎⁎ 0.037 0.025⁎⁎

053 0.032 0.056 0.009

1; df, degrees of freedom.

Fig. 3. Percentage contribution of each fish species to each sampling month ranked by their relative contribution from the SIMPER similaritypercentage analysis.

189S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

C. julis was fairly constant throughout the year (8.2–8.6 cm TL), except in December (less than 8 cm TL).For D. annularis all the between-months comparisonsshowed significant differences (pb0.005; TL range:4.9–7.9 cm), except for January that did not differfrom March and December, suggesting homogeneity insize classes during winter period (4.9–5.6 cm TL rangefor these three months). Additionally, the smallest sizesof D. annularis were in May and July (Fig. 6),matching with the recruitment season in the area. S.ocellatus showed differences between months, withlarger mean size during May and April (6.9 cm TL),

Fig. 4. Mean fish length (total length in cm) for the six m

and smaller sizes during winter (pN0.1; TL range:4.9–5.6 cm for the December–March period). S.rostratus also displayed a larger mean size duringMay (8.5 cm), with significant differences betweenMay and the remaining months (K–S test, pb0.005).For S. scriba, the lowest mean size corresponded toMay (9.8 cm), and the largest size to July (11.4 cm)with significant differences for these two months (K–Stest, pb0.025). For S. porcus, the maximum mean sizewas observed in July (11.4 cm), being this month theonly one that showed significant differences in size(pb0.025).

ost abundant fish species at each sampling month.

Fig. 6. Seasonal trends of (a) total individuals N, (b) total species s, (c) Shann(f) Simpson diversity index 1-lambda′. Solid line represents Camp de Mar locerror.

Fig. 5. Normalized Biomass Spectra for the seven sampled months.

190 S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

3.4. Seasonal changes in Normalized Biomass Spectra

Twelve fish species (those accounting for at least90% of the whole biomass) were included in the analysisof the community Normalized Biomass Spectra (NBS):C. julis, C. chromis, D. annularis, G. cruentatus, Lab-rus viridis, S. porcus, S. scrofa, S. scriba, S. mediterra-neus, S. ocellatus, S. rostratus and S. tinca. For eachmonth, the size spectra showed a peak at the size class 21

(2 g) (Fig. 5). The size classes of the fish specimensranged from class 20 (1 g) to class 28 (256 g), except inJanuary, May, September and December, with anincrease in class 29 (512 g). Excluding the values tothe left of the mode, the regressions were significant inall the cases (pb0.01), although with low r2 values(range: 0.69–0.75). The slopes did not show significant

on diversity index H′, (d) species richness d, (e) Pielou's eveness j′ andation and the dotted line Malgrats location. Error bars stand for standard

Table 3SIMPER average similarity (italics) and average dissimilarity of thefeeding guilds

IS IF CS FS HC HF PS

IS 35.3 – – – – – –IF 69.02 31.6 – – – – –CS 90.51 76.21 – – – – –FS 45.26 62.38 89.98 55.78 – – –HC 72.93 61.12 100 76.74 – – –HF 86.67 92.02 100 76.15 100 – –PS 88.98 90.02 100 79.76 100 100 –

IS=strictly invertebrate feeders, IF= invertebrate feeders/fish feeders,CS=carnivorous feeders, FS=strictly fish feeders, HC=herbivorous/carnivorous feeders, HF=herbivore strict, PS=strictly planktivorousfeeders.

191S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

differences between the seven months (ANCOVA,F=0.04, pN0.5), although being slightly smoother forthose months that showed individuals larger than the 28

class, indicating a slight increase in the biomasstowards the right side of the plot (i.e., larger individualsor species). For the class 20 (1 g), May and Julypresented lower biomass values, indicating a lowercontribution of small individuals of the species includedin the analysis.

Fig. 7. Redundancy analysis biplot showing the contribution of fish species toand abbreviations for the following fish species, Cj: Coris julis, Da: DiplMullus surmuletus, Sc: Symphodus cinereus, Sd: Symphodus doderleinmediterraneus, So: Symphodus ocellatus, Sp: Scorpaena porcus, Sr: Sympho

3.5. Species richness and diversity

The number of species ranged between 5 in Januaryand 21 in July while the total number of individuals was293 in July and 21 in September, and Margalef diversityindex differed between 4.11 in July and 1.3 in January(Fig. 6).

The pattern of variation in both locations was verysimilar in the different seasons. No significant dif-ferences were found between the two locations interms of univariate indices of diversity (Mann–Whit-ney, pN0.05) neither for the number of species, thespecies richness, the Shannon diversity index nor theequitativity.

3.6. Functional guilds

There were seasonal differences in the trophic rolesof the fish communities at seagrass meadows (SIM-PER). The similarity values within each feeding guildwere low and the dissimilarity ones ranged between 54and 100 (Table 3). The highest dissimilarities werefound among CS-HC, CS.HF, CS-PS, HC-HF, HC-PSand HF-PS.

the differences between depth and months. Triangles represent monthsodus annularis, Dv: Diplodus vulgaris, Gc: Gobius cruentatus, Ms:i, Sec: Serranus cabrilla, Ses: Serranus scriba, Sm: Symphodusdus rostratus, St: Symphodus tinca, Syt: Syngnathus typhle.

192 S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

3.7. Multivariate descriptors

The multivariate analyses (RDA) showed that depthhas a significant effect on the abundance of some fishspecies such as S. scriba and S. cabrilla (Fig. 7). Thevariability in fish composition is also affected by theseasonality as indicated by the biplot (Fig. 7). Thevariables that were significant in the RDA were depth-related effects (RDA, F=2.971; p=0.003), the interac-tion locality⁎ season-related effects (RDA, F=2.019;p=0.039) and the month-effect (RDA, F=3.087;p=0.0001).

4. Discussion

Seasonal patterns in the fish assemblages of thestudied P. oceanica seagrass meadows are clearlyenvisaged. Species richness, diversity, evenness anddensity of necto-benthic species displayed a seasonalvariation, with high values in July and low in January.These results agree with data on Posidonia seagrassbeds elsewhere (Jimenez et al., 1997) and fish fauna atother Mediterranean small-size seagrass meadows suchas Cymodocea nodosa and Zostera noltii although theseasonal patterns exhibited larger values from latespring to early autumn (Guidetti and Bussotti, 2000).Some of the seasonal changes observed may be linked tothe recruitment cycle or to strong seasonality correlatedwith reproductive aggregations (Boops boops). Bussottiand Guidetti (1999) showed that juveniles of Labridaesettled and inhabit the same habitat occupied by adults.This pattern is consistent with the data reported for otherlabrid fishes in and outside the Mediterranean basin(Garcia-Rubies and Macpherson, 1995; Green, 1996),which usually do not show any distinct ontogeneticshifts in habitat use. However, recruitment peaks forjuvenile Sparidae D. annularis and S. cantharus arereported in August (Guidetti and Bussotti, 1997). Otherstudies suggest that some species closely linked toseagrass habitats (i.e., Syngnathus argus) undergo size-related migrations from one seagrass habitat to another(Kendrick and Hyndes, 2003). From our data it seemsthat the fish communities profit from shelter and foodsupply provided by seagrass habitats for the develop-ment of their entire life cycle.

Species composition is similar to that obtained byprevious authors at P. oceanica seagrass beds at theWestern Mediterranean (Bell and Harmelin-Vivien,1982; Reñones et al., 1995; Jimenez et al., 1997; Valleet al., 2001). Total number of species in our study (51species) is slightly lower than the 53 species observedby (Valle et al., 2001), but higher than those reported by

other authors in similar habitats. The fish community ischaracterized by species belonging to the familiesLabridae, Sparidae, Serranidae, Pomacentridae, Scor-paenidae, Gobidae, Syngnathidae, and Mullidae indecreasing order of abundance. Labridae and Sparidaeare the dominant families at P. oceanica seagrass bedsas confirmed by previous studies at Western Mediterra-nean seagrass areas (Bell and Harmelin-Vivien, 1982;Harmelin-Vivien, 1983; Reñones et al., 1995; Sanchez-Jerez and Ramos-Espla, 1996; Francour, 1997; Frau etal., 2003; Deudero and Frau, 2004). Main species at thedeep seagrass beds were S. scriba, S. rostratus, S.ocellatus, D. annularis and C. julis as recorded by Valleet al. (2001) and Deudero and Frau (2004). The lowdensities of Pomacentridae and Centracanthidae speciesat our study may be explained by the sampling geardeployed since catches from beam trawl are biasedtowards species that are closely related to the substrate(Hyndes et al., 2003), capturing larger individuals andsampling fast-swimming species (Heithaus, 2004).

Length–frequency distributions obtained along theone-year cycle showed that larger sizes were collectedfrom May to July. The majority of species recorded atthe two sampling sites were represented by small-sizespecimens of an average size between 10 and 20 cmtotal length and presented a mimetism with the seagrasscanopy (Harmelin-Vivien, 1983). The results indicate asimilar population size structure between months for thefull study period, except for the dynamics of juveniles.The dominance of intermediate size classes during theyear and the scarcity or absence of large-size fish may bedue to a high mortality rate, increased swimmingactivity (i.e., foraging or reproduction) in the warmerseason or to seasonal displacements, as observed forother Labridae and Sparidae species (Francour, 1997;Bussotti and Guidetti, 1999). Gregarious species, suchas Oblada melanura and Atherina sp., although knownto be abundant in the water column above the canopywere not present in our study, probably due to gearselectivity. Juveniles of other species appear to bestrongly linked to the canopy on the margins of the‘matte’ of P. oceanica such as C. chromis (Guidetti andBussotti, 1998). The presence of C. chromis is constantalong the year, however the edge effect in our study hasnot been addressed.

In our study, long-living species (e.g., S. cabrilla, S.scriba, S. cantharus) displayed lower density variations,i.e., higher inertia, that short living species (e.g., S.ocellatus, S. rostratus, S. tinca) as shown by the resultsof the three-way ANOVA. Therefore, there seems to bea resilience of the fish assemblage. Similarly, regardingthe buffer effect, Francour (2000) points out that the

193S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

level of variation of the total fish assemblage density atCorsican waters (W Mediterranean) is lower than thoseof the main families (Labridae, Sparidae and Serrani-dae). Moreover, there are higher densities of predators inprotected seagrass beds (e.g., Serranidae) that may beindicating that the buffer effect can be linked to anincrease in predation pressure and fishing restrictions.Seagrass beds provide a foraging habitat for a diverseassemblage of predatory fish, many of which arepiscivorous as it is the case for many serranids. Anti-predator behaviour and among-location variability inabundances of piscivorous fishes may explain some ofthe diel, tidal, and broad-scale spatial patterns in small-fish abundance (Hindell et al., 2000). The presence offish belonging to the Syngnathidae family throughoutthe year shows the habitat preference of these speciestowards seagrass beds. The occurrence of syngnathids inthis specific habitat most likely reflects their ability toeffectively avoid predators by remaining camouflage.However, the pipefish densities are rather low indicatinga regression process in the studied Mallorcan seagrassbeds when compared with other pristine ones (Hecket al., 2003).

The lack of significant differences between months inthe Normalized Biomass Spectra suggests that the sizestructure for the P. oceanica fish assemblage remainsfairly constant throughout the year, at least for the sizeclasses 21 (2 g) and larger. However, for the smallerclass analysed (20), some differences appeared in Mayand July suggesting a lower contribution of the smallestindividuals during those months. Factors such asrecruitment dynamics of the main species in terms ofrelative density (i.e., C. julis, D. annularis, S. scriba, S.ocellatus and S. rostratus), different shelter capacityprovided by the coverage of the meadows, or fishingefficiency of the beam trawl used for sampling maydetermine the size structure of the fish community.Additionally, fishing pressure could also be involved inthe fish assemblage structure, since some of the mainspecies such as S. scriba, C. julis, S. tinca and D.annularis are targeted species of the recreational fisheryover P. oceanica meadows in Mallorca (Morales-Ninet al., 2005). In this sense, fishing activity could play arole affecting both species-specific density and fish sizestructure.

The composition of the fish assemblage based ondietary preference guilds indicates the dominance ofspecies which feed on invertebrates and on invertebratesand fish. This result appears to be consistent withMathieson et al. (2000) regarding the European tidalmarshes, given that a low percentage of carnivorousguilds was found in the present study (FS and CS, about

2–3% of the species). However, piscivorous speciescould be more frequent at these deeper seagrass beds ascorroborated by the relative high densities of Scorpae-nidae (S. porcus, S. scrofa) and Serranidae (S. cabrilla,S. scriba) species.

In general, timing of seasonal patterns in seagrassfish abundance, biomass, richness, and compositionpreviously has been attributed primarily to abioticinfluences. Habitat heterogeneity and structure ofvegetated systems in terms of seagrass coverage andspatial heterogeneity (e.g., shoot density) are often citedas a major factor affecting fish community in seagrassmeadows (Guidetti and Bussotti, 2002). Heck et al.(2003) reviewing the nursery role of seagrasses suggestthat structure “per se”, rather than the type of structure,appears important in determining nursery effects. Thestudy on effects of seagrass canopy removal on fish inshallow Mediterranean seagrass (C. nodosa and Z.noltii) meadows reveals that species richness, total fishabundance, and densities of Atherinidae, Diplodussargus and S. salpa were unaffected by habitat type(Guidetti and Bussotti, 2002). The seagrass leaf canopywas most important for small-size species S. ocellatus,L. viridis, D. annularis and Sparus aurata. In ourstudy, most of the species have a high affinity for theseagrass beds although the occurrence of species such asGobiids (G. cruentatus, G. bucchichi, Gobius falax, G.paganellus) suggests that part of the substrate wascovered by patches of seagrass among bare sandintensifying edge effects.

Depth effects on fish communities in seagrassmeadows are not obvious. Previous studies show thatdeep seagrass had significantly more species and higherbiomass of fish than shallow seagrass areas (Heithaus,2004). This result is consistent with Bell et al. (1992)that found deep P. australis beds supporting fishcommunities with more individuals and species thanshallow seagrass beds in Australia. However, Traversand Potter (2002) found that nearshore seagrass hadhigher fish density and diversity than offshore (deeper)seagrass. Our results suggest that deep seagrass bedssupport high number of species, abundances andbiomass especially during the summer period.

In conclusion, the seasonal variability of littoralfishes at deep P. oceanica meadows has been demon-strated indicating that seagrass beds have a fundamentalrole in maintaining populations of littoral fish andinvertebrate species by providing a permanent habitat,allowing completion of the full life cycle, a temporarynursery area, a feeding area for various life-historystages and a shelter from predation. While long-termdata are scarce, the results of this one-year cycle provide

194 S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

useful information on fish assemblages of seagrass bedsemphasising the important role exerted by deep seagrasshabitats for different fish species, as observed atvegetated systems elsewhere stressing the need for acorrect coastal zone management. Long-term surveystogether with more geographically extended areas arenecessary to support conclusions on the dynamics ofcoastal fish assemblages at temperate deep seagrasses.

Acknowledgements

The authors are mostly indebted with F. Alvarez andP. Sanchez from the Centre Oceanogràfic de Balears,Instituto Español de Oceanografía for the boat facilitiesand their availability in field work and sampling. Manythanks to T. Box, C. Alonso, P. Sarriera for field andlaboratory sampling, and P. Alos for revision of themanuscript. This study was financed by the Universitatde les Illes Balears (UIB 2002/4).

References

Bell, J.D., Harmelin-Vivien, M.L., 1982. Fish fauna of FrenchMediterranean Posidonia oceanica meadows. 1. Communitystructure. Tethys 10, 337–347.

Bell, J.D., Harmelin-Vivien, M.L., 1983. Fish fauna of FrenchMediterranean Posidonia oceanica meadows. 2. Feeding habits.Tethys 11, 1–14.

Bell, J.D., Westoby, M., 1986. Importance of local changes in leafheight and density over a wide spatial scale: effects on commonfish and decapods. J. Exp. Biol. Ecol. 104, 274–294.

Bell, J.D., Ferrell, D.J., McNeill, S.E., Worthington, D.G., 1992.Variation in assemblages of fish associated with deep and shallowmargins of the seagrass Posidonia australis. Mar. Biol. 114,667–676.

Bethoux, J.P., Copin-Montegut, G., 1986. Biological fixation ofatmospheric nitrogen in the Mediterranean Sea. Limnol. Oceanogr.31 (6), 1353–1358.

Bussotti, S., Guidetti, P., 1999. Fish communities associated withdifferent seagrass systems in the Mediterranean Sea. Nat. Siciliano23, 245–259.

Clarke, K.R., Gorley, R.N., 2001. PRIMER v5: User Manual/Tutorial.PRIMER-E, Plymouth, 91 pp.

Clarke, K.R., Warwick, R.M., 1994. Changes in Marine Communities:an Approach to Statistical Analysis and Interpretation. PlymouthMarine Laboratory, Plymouth. 144 pp.

Deudero, S., Frau, A., 2004. Role of mixed and fragmentated habitatsin fish habitat preference. CIESM Rapp. Comm. Int. Mer. Médit.37, 513.

Deudero, S., Pinnegar, J.K., Polunin, N.V.C., Morey, G., Morales-Nin,B., 2004. Spatial variation and ontogenic shifts in the isotopiccomposition of Mediterranean littoral fishes. Mar. Biol. 145,971–981.

Ferrell, D.J., McNeill, S.E., Worthington, D.G., Bell, J.D., 1993.Temporal and Spatial Variation in the Abundance of FishAssociated with the Seagrass Posidonia Australis in South-EasternAustralia. Aust. J. Mar. Freshw. Res. 44, 881–899.

Francour, P., 1994. Pluriannual analysis of the reserve effect onichthyofauna in the Scandola natural reserve (Corsica, North-western mediterranean). Oceanol. Acta 17, 309–317.

Francour, P., 1997. Fish assemblages of Posidonia oceanica beds atPort Cros (France, NWMediterranean): assessment of compositionand long-term fluctuations by visual census. Marine Ecology-Pubblicazioni della stazione zoologica di Napoli I 18, 157–173.

Francour, P., 2000. Long term monitoring of Posidonia oceanica fishassemblages of the Scandola Marine Reserve (Corsica, north-western Mediterranean). Cybium 24, 85–95.

Frau, A., Deudero, S., Cerdeño, S., Alou, L., 2003. No habitatpreference in mixed meadows and rocky bottoms in MediterraneanLabridae and Sparidae fish species. Boletín del Instituto Españolde 19 (1–4), 483–491.

Garcia-Rubies, A., Macpherson, E., 1995. Substrate use and temporalpattern of recruitment in juvenile fishes of the Mediterraneanlittoral. Mar. Biol. 124, 35–42.

Green, A.L., 1996. Spatial, temporal and ontogenetic patterns ofhabitat use by coral reef fishes (Family Labridae). Mar. Ecol., Prog.Ser. 133, 1–11.

Guest, M.A., Connolly, R.M., Loneragan, N.R., 2003. Seine netsand beam trawls compared by day and night for sampling fishand crustaceans in shallow seagrass habitat. Fish. Res. 64,185–196.

Guidetti, P., Bussotti, S., 1997. Recruitment of Diplodus annularis andSpondyliosoma cantharus (Sparidae) in shalllow seagrass bedsalong the Italian coasts (Mediterranean Sea). Mar. Life 7, 47–52.

Guidetti, P., Bussotti, S., 1998. Juveniles of littoral fish species inshallow seagrass beds: preliminary quali-quantitative data. Biol.Mar. Mediterr. 5, 347–350.

Guidetti, P., Bussotti, S., 2000. Fish fauna of a mixed meadowcomposed by the seagrasses Cymodocea nodosa and Zostera noltiiin the Western Mediterranean. Oceanol. Acta 23, 759–770.

Guidetti, P., Bussotti, S., 2002. Effects of seagrass canopy removal onfish in shallow Mediterranean seagrass (Cymodocea nodosa andZostera noltii) meadows: a local-scale approach. Mar. Biol. 140,445–453.

Guidetti, P., Fabiano, M., 2000. The use of lepidochronology to assessthe impact of terrigenous discharges on the primary leaf productionof the Mediterranean seagrass Posidonia oceanica. Mar. Pollut.Bull. 40, 449–453.

Guillen, J.E., Ramos, A.A., Martinez, L., Lizaso, J.L.S., 1994.Antitrawling Reefs and the Protection of Posidonia oceanica (L)Delile Meadows in the Western Mediterranean-Sea—Demand andAims. Bull. Mar. Sci. 55, 645–650.

Harmelin-Vivien, M.L., 1983. Ichthyofaune des herbiers de posidoniesdes cotes provençales françaises. Rapp. Comm. Int. Mer. Médit.28, 161–163.

Harmelin-Vivien, M.L., Francour, P., 1992. Trawling or visualcensuses? Methodological bias in the assessment of fish popula-tions in seagrass beds. P.S.Z.N. I: Mar. Ecol. 13 (1), 41–51.

Harmelin-Vivien, M.L., Harmelin, J.C., Chauvet, C., Duval, C.,Galzin, R., Lejeune, P., Barnabe, G., Blanc, F., Chevalier, R.,Duclerc, J., Lassere, G., 1985. Evaluation visuelle des peuplementset populations de poisons: problémes et méthodes. Rev. Ecol.(Terre Vie) 40, 467–539.

Heck, K.L., Hays, G., Orth, R.J., 2003. Critical evaluation of thenursery role hypothesis for seagrass meadows. Mar. Ecol., Progr.Ser. 253, 123–136.

Heithaus, M.R., 2004. Fish communities of subtropical seagrassmeadows and associated habitats in Shark Bay, Western Australia.Bull. Mar. Sci. 75, 79–99.

195S. Deudero et al. / Journal of Marine Systems 70 (2008) 182–195

Hindell, J.S., Jenkins, G.P., Keough, M.J., 2000. Variability inabundances of fishes associated with seagrass habitats in relationto diets of predatory fishes. Mar. Biol. 136, 725–737.

Howard, R.K., 1987. Diel variation in the abundance of epifaunaassociated with seagrasses of the Indian River, Florida, USA. Mar.Biol. 96, 137–142.

Hyndes, G.A., Kendrick, A.J., MacArthur, L.D., Stewart, E., 2003.Differences in the species- and size-composition of fish assem-blages in three distinct seagrass habitats with differing plant andmeadow structure. Mar. Biol. 142, 1195–1206.

Jackson, E.L., Rowden, A.A., Attrill, M.J., Bossey, S.J., Jones, M.B.,2001. The importance of seagrass beds as a habitat for fisheryspecies. Oceanography and Mar. Biol., vol. 39, pp. 269–303.

Jimenez, S., Bayle, J.T., Ramos Espla, A.A., Sanchez-Lisazo, J.L.,1997. Ictiofauna de dos praderas de Posidonia oceanica (L.)Delile, 1813 con distinto grado de conservacion. PublicacionesEspeciales Instituto Español de Oceanografia 23, 255–264.

Kendrick, A.J., Hyndes, G.A., 2003. Patterns in the abundance andsize-distribution of syngnathid fishes among habitats in a seagrass-dominated marine environment. Estuar. Coast. Shelf Sci. 57,631–640.

Lipej, L., Bonaca, M.O., Sisko, M., 2003. Coastal fish diversity inthree marine protected areas and one unprotected area in the Gulfof Trieste (Northern Adriatic). Mar. Ecol. 24, 259–273.

Macpherson, E., Gordoa, A., 1996. Biomass spectra in benthic fishassemblages in the Benguela System. Mar. Ecol., Progr. Ser. 138,27–32.

Macpherson, E., Gordoa, A., García-Rubies, A., 2002. Biomass sizespectra in littoral fishes in protected and unprotected areas in theNW Mediterranean. Estuar. Coast. Shelf Sci. 55, 777–788.

Malavasi, S., Fiorin, R., Franco, A., Franzoi, P., Granzotto, A.,Riccato, F., Mainardi, D., 2004. Fish assemblages of VeniceLagoon shallow waters: an analysis based on species, families andfunctional guilds. J. Mar. Syst. 51, 19–31.

Marbà, N., Duarte, C.M., 1997. Interannual changes in seagrass(Posidonia oceanica) growth and environmental change in theSpanish Mediterranean littoral. Limnol. Oceanogr. 42, 800–810.

Mas, J., Franco, I., Barcala, E., 1993. Primera aproximación a lacartografía de las praderas de Posidonia oceanica en las costasmediterráneas españolas.factores de alteración y de regresión.Legislación. Publ. Espec. Inst.Esp. Oceanogr. 11, 111–122.

Massutí, M., 1965. Estudio de los fondos de pesca de Baleares. Nota1a. Ciclo anual de los peces de las praderas de Caulerpa yPosidonia capturados por un pequeño arte de arrastre en la bahía dePalma de Mallorca. Bol. Inst. Esp. Oceanogr. 119, 1–57.

Mathieson, S., Carttrijsse, A., Costa, M.J., Drake, P., Elliott, M.,Gardner, J., MArchand, J., 2000. Fish assemblages of Europeantidal marshes: a comparison based on species, families andfunctional guilds. Mar. Ecol., Progr. Ser. 204, 225–242.

Morales-Nin, B., Moranta, J., Garcia, C., Tugores, M.P., Grau, A.M.,Riera, F., Cerda, M., 2005. The recreational fishery off MajorcaIsland (western Mediterranean): some implications for coastalresource management. Ices J. Mar. Sci. 62 (4), 727–739.

Petrik, R., Levin, P.S., 2000. Estimating relative abundance of seagrassfishes: a quantitative comparison of three methods. Environ. Biol.Fishes 58, 461–466.

Platt, T., Denman, K.L., 1978. The structure of pelagic marineecosystems. Rapp. P.-V. Reun. Cons. Int. Explor. Mer. 173, 60–65.

Proccacini, G., Buia, M.C., Gambi, M.C., Pérez, M., Pergent, G.,Pergent-Martini, C., Romero, J., 2003. The seagrass of the westernMediterranean. In: Green, E.P., Short, F.T. (Eds.), World Atlas ofSeagrasses: Present Status and Future Conservation. University ofCalifornia Press, Berkeley, pp. 48–58.

Reñones, O., Massuti, E., Moranta, J., Coll, J., Moreno, I., 1995. Fishfauna of Posidonia oceanica seagrass meadows in Palma bay(Balearic Islands). Cybium 19, 201–206.

Sanchez-Jerez, P., Ramos-Espla, A.A., 1996. Detection of environ-mental impacts by bottom trawling on Posidonia oceanica (L.)Delille meadows: sensitive of fish and macroinvertebrate commu-nities. J. Ecosyst. Health 5, 239–253.

Sanchez-Jerez, P., Ramos-Espla, A., 2000. Changes in fish assem-blages associated with the deployment of an antitrawling reef inseagrass meadows. Trans. Am. Fish. Soc. 129, 1150–1159.

Short, F.T., Wyllie-Echevarria, S., 1996. Natural and human-induceddisturbance of seagrasses. Environ. Conserv. 23, 17–27.

Tanner, J.E., 2005. Edge effects on fauna in fragmented seagrassmeadows. Aust. Ecol. 30, 210–218.

ter Braak, C.J.F., Smilauer, P., 2002. CANOCO Reference Manual andUser's Guide to Canoco for Windows: Software for CanonicalCommunity Ordination (version 4.5). Microcomputer Power,Ithaca, NY, USA.

Travers, M.J., Potter, I.C., 2002. Factors influencing the characteristicsof fish assemblages in a large subtropical marine embayment.J. Fish Biol. 61, 764–784.

Valle, C., Bayle Sempere, J.T., Ramos Espla, A.A., 2001. Estudiomultiescalar de la ictiofauna asociada a praderas de Posidoniaoceanica (L.) Delile, 1813 en Alicante (sudeste iberico). BoletinEspañol de Oceanografia 17, 49–60.