Impact of an open-sea suspended mussel culture on macrobenthic community (Western Adriatic Sea)

Aquaculture 289 (2009) 54–63

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Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e

Impact of an open-sea suspended mussel culture on macrobenthic community (Western Adriatic Sea) Gianna Fabi, Sarine Manoukian ⁎, Alessandra Spagnolo CNR-Istituto di Scienze Marine, Sede di Ancona, Largo Fiera della Pesca, 60125 Ancona, Italy

a r t i c l e

i n f o

Article history: Received 13 February 2008 Received in revised form 18 December 2008 Accepted 18 December 2008 Keywords: Mariculture impact Mussel culture Macrobenthic community Open-sea Adriatic Sea

a b s t r a c t The potential impact of a suspended mussel farm on the coastal macrobenthic communities of the Western Adriatic Sea was seasonally evaluated through a multi-control sampling strategy over 1 year. Both univariate biological indices and multivariate analysis indicated that the variations of benthic macrofauna were mainly due to seasonality rather than location of the sampling sites in respect to the farm, and that the main species contributors were common to most sites and seasons. Most of these species are known as indicators of organic enrichment and/or pioneer species in recolonization of defaunated bottoms and commonly occur in the macrobenthic populations inhabiting the seabed of the North-Central Adriatic Sea between 12 and 15 m depth. Only the different abundances of filter- and deposit-feeders gave some evidence of a limited, spatial influence on the culture in the surroundings. The external sites showed a significant difference compared to the reference sites (ANOSIM: R = 0.395, P = 0.5). The overall results suggest that open-sea mussel culture has minimal detrimental effects on the zoobenthic communities of the Western Adriatic Sea that are usually in an immature stage due to subsequent environmental and anthropogenic disturbances. Although one-year study might not be sufficient to evaluate the effects of mussel culture, the results of this work represent a useful tool for the monitoring of the potential environmental impact of mussel farms to ensure the sustainable development of shellfish culture in the Italian shallow coastal waters. © 2009 Elsevier B.V. All rights reserved.

1. Introduction In Italy commercial farming of shellfish has always played the most important role in marine and brackish water aquaculture from the viewpoint of productivity, areal exploitation and number of farms. Mussel farming (Mytilus galloprovincialis) represents the most important activity and it noticeably increased in the last 15 years. The most recent Italian census points out that in 2005 there were 263 mussel cultures (Prioli, 2008), while the annual production amounted to around 63,500 t corresponding nearly to 50% of the national shellfish culture production (FAO FISHSTAT, 2005). In the past, most of these cultures consisted of floating or bottom systems localized in sheltered areas (bays, gulfs, lagoons) but recently a lot of new longline farms have been established in the open sea, mainly along the Italian coast of the Northern and Central Adriatic Sea, where the high hydrodynamism enhances mussel growth (Maffei et al., 1996) and minimizes the possible environmental impacts inducing a greater dilution of faecal and pseudo-faecal material (Midlen and Redding, 1998; Muir, 2001; Hartstein and Rowden, 2004). Intensive shellfish farming, in fact, involves large amounts of organic material accumulation on the bottom below the cultures ⁎ Corresponding author. Tel.: +39 340 4039274; fax: +39 071 55313. E-mail addresses: [email protected] (G. Fabi), [email protected] (S. Manoukian), [email protected] (A. Spagnolo). 0044-8486/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2008.12.026

causing strong changes in the physical and chemical characteristics of sediments (Dahlback and Gunnarsson, 1981; Kaspar et al., 1985; Gilbert et al., 1997; Nizzoli et al., 2006). A variety of levels of effect of suspended mussel culture on the benthic marine environment are reported in literature (Tenore et al., 1982; Kaspar et al., 1985; Baudinet et al., 1990; Hargrave, 1994). Heavy sedimentation of organic material directly below mussel farms leads to localised enrichment inducing oxygen depletion and sulphate reduction in areas with poor water exchange (Dahlback and Gunnarsson, 1981; Kaspar et al., 1985; Dowd, 2005; Giles et al., 2006) altering bacteria and benthic environments (Castel et al., 1989; Dinet et al., 1990; Grenz et al., 1990; Duplisea and Hargrave, 1996). Macrofaunal abundance is commonly reduced (Tenore et al., 1982; Mattsson and Lindén, 1983; Grant et al., 1995; Beadman et al., 2004; Smith and Shackley, 2004; da Costa and Nalesso, 2006) and differences in the composition of the infauna population are observed with a larger diversity at the reference sites (Kaspar et al., 1985), while opportunistic deposit-feeders dominate the benthic infauna of the mussel-farm sediment (Dahlback and Gunnarsson, 1981; Mattsson and Lindén, 1983; Smaal, 1991; Munday et al., 1992; Grant et al., 1995). Similar but weaker effects have also been observed in some of the few studies carried out in this field in the Mediterranean Sea, i.e. in the Gulf of Trieste and in the Gulf of Gaeta (Brizzi et al., 1995; Mirto et al., 2000). The long-term sustainability of shellfish farming depends on the maintenance of the health of the natural ecosystem and evaluating the

G. Fabi et al. / Aquaculture 289 (2009) 54–63

effects of suspended mussel cultures on the underlying marine environment; the benthic community is a primary factor in determining the sustainable environmental management of aquaculture (Gibbs, 2007). Systematic monitoring of marine ecosystem is extremely important to detect physical, chemical and biological changes in the water column, sediments and above all in the benthic community that can include highly sensitive species to ecological alteration caused by mussel bioturbation (Mirto et al., 2000). Indicator species usually tolerate adverse sediment conditions and may be represented by a wide variety of taxa (Pearson et al., 1983; Smith et al., 2001). Therefore, while microbial communities have been suggested as bioindicators for their important role in the biogeochemical processes occurring in mussel farm sediments (La Rosa et al., 2001), meio and macrofauna have been proposed as new environmental bioindicators of mussel farm impacted areas due to their ability to sensitively respond to any ecological alteration caused by organic enrichment (Mazzola et al., 1999, Mirto et al., 1999, da Costa and Nalesso, 2006). However, most of the available literature refers to intensive mussel cultures in estuaries and inshore coastal waters, while very little is known about the offshore farms. Therefore, the present study was developed to provide baseline biological information on the effects of open-sea suspended cultures of M. galloprovincialis on the macrobenthic communities of the North-Central Adriatic Sea, in order to evaluate its seasonal impact. 2. Methods 2.1. Sample sites A mussel culture located at about 2.5 km offshore the Western Adriatic coast at a mean depth of 11 m on a sandy-mud seabed, was

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investigated from June 2001 to February 2002 (Fig. 1). The farm was built in 1995 and production started in 1996. It takes up an area of 2 km2 with 27 horizontal long-lines from 900 to 1600 m of length placed at 40–50 m from each other. The 2.5–3 m vertical long strings holding the mussels and bounded to the horizontal long-lines are 3–5 m above the bottom. The production is about 1000 t yr− 1. The long-lines are Southeast oriented, running parallel to the shoreline and to the predominant Southeast current that has a mean speed of 10 cm s− 1 and maximum speed of 30 cm s− 1. Detailed studies on water circulation in the area were carried out by Artegiani et al. (1997) and Gačić and Artegiani (2001). The sandy-mud sediments of the mussel culture area were described by Danovaro et al. (2004). They reported seasonal variations in grain size composition with an increment of the sand/mud fraction in spring and fall. Redox potential discontinuity depth also varied widely between the seasons, ranging from 0.7 cm in summer to 6.5 cm in winter, while the total organic matter showed values between 1.2 ± 0.1 (summer) and 6.1 ± 3.3% (winter) of sediment dried weight. 2.2. Data collection A preliminary survey was carried out in April 2001 and nine sites were selected for benthic sampling within and surrounding the mussel farm (Fig. 1). Two sites, I1 and I2 were inside the farm boundary and two sites were established as controls 600 m to the Northwest and West (C1 and C2). To study the possible effects of the farm over a linear gradient, sites E0, E1, E2, E3, and E4 were located along a Southeast axis parallel to the main current direction, extending 0, 30, 60, 120, and 300 m from the farm, respectively. Four monitoring surveys were carried out with consideration of selected environmental and farming factors: the first one was

Fig. 1. Location of the mussel farm along the Western Adriatic coast and sampling scheme. C1 and C2: control sites; I1 and I2: inside farm sites; OT: outside transect; E0, E1, E2, E3 and E4: outside transect sites.

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Fig. 2. Univariate indices of macrofaunal community structure at each sampling site in each season. S = total species richness; Sm = mean (± SE) species richness per station; N = mean (±SE) abundance per station; d = mean (±SE) Margalef species richness per station; H' = mean (± SE) Shannon diversity index per station; J' = mean (± SE) evenness index per station. Other abbreviations as in Fig. 1.

conducted in late spring 2001 (June) after the emptying of the culture; the second survey in late summer 2001 (September), when the culture was in the half-load phase; the third and the last ones were carried out in fall 2001 (December) and winter 2002 (February) in correspondence to the largest biomass of mussels inside the farm and the high water column mixing. At each site, three samples were collected using a Van-Veen grab (13 L; 0.105 m2), partitioned in situ using a 0.5 mm mesh sieve and preserved in 5% buffered formalin to be analyzed in the lab. The macrofauna was sorted through a stereo- and a binocular microscope, identified to the lowest taxonomic level possible, quantified and weighed. 2.3. Data analysis Benthic community data were standardized to dm2 and then processed using both univariate and multivariate statistical analyses. Total species richness (S) was computed as the total number of species collected at each sampling site in each season. Mean abundance (number of individuals dm− 2; N), mean number of species (Sm), Margalef species richness (d; Margalef, 1963, 1968), Shannon diversity (H'; calculated using base-10 logarithms; Pielou, 1974) and Pielou's evenness (J'; Pielou, 1974) were also calculated per season and sampling site.

Multiple comparisons of these indices among a priori grouping sites and seasons were performed using a two-way ANOVA (Lindman, 1992) and testing variances normality and homogeneity hypothesis through the Kolmogorov–Smirnov and Bartlett tests, respectively (Lindman, 1992). Grouping of the sampling sites was performed on the basis of their location in respect to the culture: inside the farm (I1 and I2; group IN), along the outside transect (E0, E1, E2, E3 and E4; group OT) and reference sites (C1 and C2; group C). Tukey HSD post hoc test was used when ANOVA test showed highly significant (P b 0.01) or significant (P b 0.05) differences. To appreciate spatial and temporal changes in species abundance, multivariate technique was applied using the PRIMER™ ecological software package developed by the Plymouth Marine Laboratory (Clarke, 1993; Clarke and Warwick, 1994). Macroinvertebrate abundance data were √ transformed to reduce the contribution of prevalent taxa and therefore increase the importance of less abundance species prior to all subsequent analyses. A ranked triangular similarity matrix was constructed using the Bray-Curtis similarity coefficient (Bray and Curtis, 1957). Ordination was computed by hierarchical agglomerative clustering using the group-average sorting (Lance and Williams, 1967) and non-metric multidimensional scaling (MDS ordination; Shepard, 1962; Kruskal, 1964a,b).

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Table 1 Results of 2-way ANOVA applied to mean values of total species richness (S), mean species richness per station (Sm), mean abundance per station (N), Margalef species richness (d), Shannon diversity index (H') and evenness index (J') computed for a priori season and site groups

Table 3 SIMPER output indicating average abundance (N dm− 2) and % contribution to % average similarity within a priori season (a) and site groups (b) of the four most important species

Variable Source of variability

df df Mean error square

Ms error

S

2 3 6 2 3 6 2 3 6 2 3 6 2 3 6 2 3 6

39.217 1.519 0.187 39.217 1.733 0.239 39.217 0.798 0.581 14.409 2.296 0.122 14.409 4.117 0.017⁎ Su b Sp, W 14.409 1.130 0.375 35.418 0.729 0.493 35.418 13.947 0.000⁎⁎ SpNN Su, F, W 35.418 1.056 0.416 3.701 1.784 0.874 3.701 0.232 0.189 3.701 0.674 0.672 0.055 0.358 0.439 0.055 0.935 0.703 0.055 0.287 0.937 0.001 0.288 0.752 0.001 3.273 0.038⁎ Sp b W 0.001 0.266 0.375

(a) Season groups across site groups Sp 79.60 Caprella equilibra Owenia fusiformis Ampelisca intermedia Corbula gibba Su 75.09 Owenia fusiformis Mysella bidentata Corbula gibba Chamelea gallina F 76.12 Owenia fusiformis Mysella bidentata Laonice cirrata Chamelea gallina W 74.43 Owenia fusiformis Mysella bidentata Aricidea capensis Corbula gibba (b) Site groups across season groups C 72.09 Owenia fusiformis Prionospio cirrifera Caprella equilibra Mysella bidentata OT 77.51 Owenia fusiformis Corbula gibba Mysella bidentata Caprella equilibra IN 68.45 Owenia fusiformis Ampelisca intermedia Caprella equilibra Iphinoe tenella

Sm

N

D

H'

J'

site season sitex season site season sitex season site season sitex season site season sitex season site season sitex season site season sitex season

24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24 24

59.600 67.978 31.304 33.093 59.331 16.285 25.838 493.981 37.394 6.602 0.855 2.496 0.019 0.051 0.016 0.0003 0.003 0.0003

F

P

Tukey's HSD

⁎⁎, NN = highly significant; ⁎, N = significant; Su = summer; Sp = spring; F = fall; W = winter.

The macrobenthic community assemblages among the seasons and the sampling sites were tested using a priori non-parametric twoway crossed analysis of similarity (ANOSIM), while one-way ANOSIM (Clarke and Green, 1988) was used to test these differences among site groups within each single season. ANOSIM assesses significant differences between groups of replicates against a series of random simulations, resulting in the calculation of a test statistic (R), which can range from −1 to 1. R will be close to 1 when replicates are very dissimilar and approach 0 as they become more similar. A very negative R-value is unusual and indicates that between-group similarity is higher than within-group similarity. Afterwards, the relative contribution of each species to the average dissimilarities of these groupings were calculated using two-way crossed similarity percentages procedure (SIMPER; Clarke, 1993), while one-way SIMPER (Clarke, 1993) was used at seasonal level. 3. Results 3.1. Univariate indices Altogether 144 taxa were identified in the whole sampling period (51 polychaetes, 45 molluscs, 33 crustaceans, 10 echinoderms and other minor groups). S ranged from 85 (E0) to 66 (I1). A variability was observed among the seasons with a general decrease in sum-

Groups

% Average similarity

N dm− 2

% Contribution

6.69 4.02 2.84 2.70

31.55 20.43 13.19 13.04

3.64 1.64 1.49 0.96

44.70 21.22 19.08 8.24

4.28 1.16 0.98 0.99

46.00 11.61 11.42 7.21

3.33 1.14 0.71 0.86

28.77 9.84 7.85 7.64

3.55 2.32 1.49 0.88

31.15 12.34 10.05 8.32

4.06 1.76 1.08 1.70

35.76 12.57 11.00 7.81

3.47 1.80 1.74 1.01

27.87 11.05 8.47 7.97

Abbreviations as in Table 1 and Figs. 1 and 5.

mer (Fig. 2a), especially at C2 and at the internal sites. In fact, a loss of several sporadic taxa of crustaceans and molluscs (e.g. Anapagurus bicorniger, Athanas nitescens, Acanthocardia tuberculata) occurred at C2, while I1 and I2 showed a loss of polychaetes and crustaceans (e.g. Ampharete acutifrons, Sternaspis scutata, Caprella equilibra). At these sites a recovery followed in fall while a further reduction characterised the other stations. Finally, S increased in winter nearly everywhere. In the overall period, Sm varied from 11.67±0.67 to 30.67±3.18 (Fig. 2b). It followed a similar trend observed for S with a general decrease in summer, which became significantly lower than spring and winter (Table 1).

Table 2 Pairwise test between a priori season (a) and site groups (b) Groups (a) season Sp–Su Sp–F Sp–W Su–F Su–W F–W (b) site C–OT C–IN OT–IN

R statistic

% Significance level

0.983 1.000 1.000 0.679 0.883 0.700

0.6⁎⁎ 0.2⁎⁎ 0.2⁎⁎ 0.2⁎⁎ 0.2⁎⁎ 0.1⁎⁎

0.395 0.000 0.218

0.5⁎⁎ 44.4 6.8

R value for each pairwise comparison is given together with the level of significance in percentage (Bonferroni correction has been carried out). A significance level of 0.8% has been kept for season groups test (a) and of 1.7% for site groups test (b). ⁎⁎ = highly significant. Abbreviations as in Table 1 and Figs. 1 and 5.

Table 4 SIMPER output indicating % average dissimilarity between a priori season (a) and site groups (b) Groups (a) season Sp–Su Sp–F Sp–W Su–F Su–W F–W (b) site C–OT C–IN OT–IN Abbreviations as in Table 1 and Figs. 1 and 5.

% Average dissimilarity 61.71 67.98 60.02 37.87 47.20 34.69 31.19 27.94 27.94

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Fig. 3. Dendrogram of hierarchical clustering using group-average linking of the 36 samples in the overall study period. The two groups of stations separated at a 49% similarity threshold (dotted line) are indicated. Abbreviations as in Fig. 1.

Highly significant differences among the seasons were also observed for N, with the greatest values in spring (Fig. 2c, Table 1) due to the large quantity of amphipods, especially C. equilibra. In the subsequent season the drastic reduction of amphipods caused a severe collapse at all stations. A certain variability was observed from summer to winter and the community inhabiting most of the sites was dominated by polychaetes, mainly represented by Owenia fusiformis. No significant differences were obtained between site groups neither for this index nor for d, H' and J' (Table 1). d index followed a positive trend from spring 2001 to winter 2002 at most of sampling stations (Fig. 2d, Table 1). From the spatial point of view certain variability occurred in spring and summer, while a greater homogeneity was observed in fall and winter. H' and J' followed very similar trends at the different sites in all seasons, although H' showed greater fluctuations (Fig. 2e and f). A homogeneity was evidenced in spring when H' ranged from 0.67 ± 0.07 (I1) to 1.00 ± 0.04 (E0) and J' from 0.43 ± 0.03 (I1) to 0.62 ± 0.04

(I2). The lowest values recorded at I1 were due to the strong dominance of C. equilibra that disappeared in summer leading to an increase of both indices. A general reduction occurred in fall when a strong dominance of O. fusiformis was observed at most of sampling stations. This polychaete dominated also in winter, but its abundance decreased inducing a general rise of H' and J'. A significant difference was only detected for J' with spring lower than winter (Table 1). 3.2. Multivariate analysis Two-way ANOSIM showed highly significant differences over the seasons (R = 0.879, P = 0.001), and the pairwise test pointed out that every season was significantly different from each other (Table 2). Significant differences were also observed among site groups (IN, OT, C) (R = 0.267, P = 0.014). Only OT resulted significantly different from C in the pairwise test (Table 2).

Fig. 4. Non-metric multi-dimensional scaling (MDS) plot in 2 dimensions for benthic macrofaunal data collected in the whole sampling period with superimposed clusters from Fig. 3, at similarity level of 49%. Abbreviations as in Fig. 1.

G. Fabi et al. / Aquaculture 289 (2009) 54–63 Table 5 SIMPER output indicating average abundance (N dm− 2) and % contribution to % average similarity within site groups in each sampling season of the four most important species Groups Sp C Caprella equilibra Owenia fusiformis Prionospio cirrifera Ampelisca intermedia OT Caprella equilibra Owenia fusiformis Corbula gibba Ampelisca intermedia IN Caprella equilibra Owenia fusiformis Iphinoe tenella Ampelisca intermedia Su C Owenia fusiformis Prionospio cirrifera Mysella bidentata Corbula gibba OT Owenia fusiformis Mysella bidentata Corbula gibba Chamelea gallina IN Chamelea gallina Owenia fusiformis Corbula gibba Prionospio cirrifera F C Owenia fusiformis Prionospio malmgreni Ostracoda nd Mysella bidentata OT Owenia fusiformis Laonice cirrata Mysella bidentata Corbula gibba IN Owenia fusiformis Ostracoda nd Aricidea capensis Mysella bidentata W C Owenia fusiformis Prionospio malmgreni Sabella pavonina Pseudolirius kroyeri OT Owenia fusiformis Mysella bidentata Aricidea capensis Corbula gibba IN Owenia fusiformis Ampelisca intermedia Laonice cirrata Iphinoe tenella

% Average similarity

N dm− 2

% Contribution

5.96 3.43 2.96 2.08

34.48 20.73 14.35 12.35

6.79 4.37 3.25 3.16

30.69 20.44 14.53 13.37

7.18 3.74 3.07 2.78

33.86 20.04 15.34 12.45

2.60 3.40 0.86 0.81

50.19 18.91 18.64 12.26

4.33 2.07 1.87 0.90

45.49 21.73 19.49 8.04

1.80 2.95 1.22 3.32

22.83 22.50 20.30 19.42

4.46 2.18 2.21 1.36

33.90 14.94 12.09 9.41

4.28 1.11 1.08 0.93

48.52 12.37 11.85 7.85

4.11 1.62 1.54 1.16

33.71 16.10 13.88 11.41

3.71 2.05 1.86 2.21

25.95 11.22 10.83 9.30

3.27 1.16 0.90 0.98

28.51 10.12 8.61 7.92

3.09 0.99 0.82 1.02

35.30 12.34 10.33 9.72

84.05

78.18

89.38

55.21

80.35

42.28

75.39

75.71

80.93

73.72

75.82

61.23

Abbreviations as in Table 1 and Figs. 1 and 5.

Two-way crossed SIMPER test showed how the benthic communities contributed to a priori groupings, indicating the main taxa abundance and contribution (Table 3). The major dissimilarities in the pairwise comparisons were obtained for seasons rather than site groups (Table 4), with spring slightly different from the others. In fact, summer, fall and winter showed at least 74% of common major

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contributors in similarity, with O. fusiformis and Mysella bidentata as the most representative (Table 3). A great similarity of the most contributor species was also revealed as regards the three site groups across all seasons (Tables 3 and 4). Cluster analysis also supported the influence of seasonality showing that at 49% of similarity level the sampling sites were gathered into two groups on the basis of season (Fig. 3). This grouping was also well outlined by MDS ordination plot (Fig. 4) where spring was clearly separated, while summer, fall and winter resulted clustered together and yet continuing to be visibly identifiable to each other (stress = 0.13). Considering each season as a separate data set, ANOSIM test did not give any significant differences among the sites in spring (R = −0.201, P = 0.823) and SIMPER analysis clearly confirmed this taxa composition similarity (Table 5). In Cluster classification the sites resulted again very similar to each other during spring (out of phase of mussel production) joining all together at a 77% of similarity level (Fig. 5). At a higher level of 84% they split into four assemblages well represented in MDS plot ordination (stress = 0.09) and mainly characterised by different abundance distributions of Corbula gibba and Ampelisca intermedia (Fig. 6), with the minimum values recorded in I1-I2-C1 cluster and the highest ones in E0-E1 cluster. Summer data outlined some changes in taxa abundance and distribution among the sites. ANOSIM analysis showed significant differences between a priori site groups (R = 0.569, P = 0.011) and post hoc test evidenced that OT was significantly different from both C (R = 0.673, P = 0.048) and IN (R = 0.709, P = 0.048). The species having the greatest contribution were nearly the same in the three groups, but their average abundance played an essential role to define the observed differences (Table 5). Cluster and MDS analysis (stress = 0.03) confirmed this result. At a similarity level of 74% all OT sites made up a unique assemblage (Figs. 5 and 6), while each inner site linked with its corresponding control (I1-C1 and I2-C2). Prionospio cirrifera, O. fusiformis and C. gibba were the major species responsible for this clustering. In fact, both OT and I2-C2 clusters were characterized by great quantities of O. fusiformis, but the former showed the highest densities of C. gibba and the latter of P. cirrifera. I1-C1 revealed the lowest abundances of each species. OT, IN and C were similar in fall (R = 0.326, P = 0.079). OT sites tended to remain in a separated cluster due to very low densities of most of taxa. Only the boundary site E0 directly jointed to IN and C at a 75% of similarity (stress = 0.08; Figs. 5 and 6) for the highest densities of Chamelea gallina, P. cirrifera and Ostracoda nd. Also in the last sampling season a certain similarity was evidenced among the site groups (R = 0.375, P = 0.063), mixing up again. At the 79% of similarity level they split into five assemblages (stress = 0.06), three of which consisting of only one sampling site, distinguished by an unequal distribution of A. intermedia, C. gibba, Laonice cirrata, P. cirrifera, and Aricidea capensis and the exclusive occurrence of some minor species of polychaetes (Figs. 5 and 6). 4. Discussion Marine farming activities can have a potentially detrimental effect on the marine environment (Tenore et al., 1982; Mattsson and Lindén, 1983; Kaspar et al., 1988; Weston, 1990; Kaiser et al., 1998; Kaiser, 2000). This is true especially for poorly executed finfish aquaculture in coastal areas due to the release of waste matter which partly disperses in the water column and partly deposits on the seabed (Christie and Moldan, 1977; Tancioni and Scardi, 2001; Fernandes et al., 2002). Shellfish culture is however expected to be less impacting than finfish farming which requires a direct input of nutrient rich feed as well as therapeutic treatments, antibiotics, hormones, antifoulants, etc. On the contrary, the majority of shellfish filter feed on phytoplankton and suspended matter naturally occurring in the water with no supplementary food or potentially harmful chemicals added (Folke and

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Fig. 5. Dendrograms of hierarchical clustering using group-average linking of the 9 samples in each season. The groups of stations separated at 84%, 74%, 75% and 79% similarity threshold (dotted line) are indicated. C: control sites; IN: inside farm sites. Other abbreviations as in Fig. 1.

Kautsky, 1989; Inglis et al., 2000; Mirto et al., 2000; Crawford, 2003). In Tasmania, for example, the effects of shellfish farming on the benthic environment under and near subtidal farms were low and far less than those observed around salmon farms (Crawford et al., 2001, 2003). Mirto et al. (2000) and La Rosa et al. (2002) revealed that mussel cultures induced a considerably lower disturbance both on water column and benthic community structure in a comparative analysis with finfish farms in the Mediterranean Sea. Furthermore, as the behaviour of any type of waste released into the water column strongly depends on the hydrographical conditions, these impacts should be much less intense in areas with great water exchange (Midlen and Redding, 1998; Crawford et al., 2003). In fact, a comparison between two mussel (Mytilus edulis) farms in Southwest Ireland indicated no alteration of the benthic community structure at the site where current velocity was higher (Chamberlain et al., 2001). Similarly, in a study conducted at high and low energy sites, Hartstein and Rowden (2004) found a relationship between the hydrodynamic regime of the farm sites, organic enrichment of seabed sediments by mussel biodeposits, and the subsequent modification of the macroinvertebrate assemblage. The above results agree with the findings of the present study aimed to evaluate the potential impact induced by open sea mussel long-lines along the Western Adriatic coast where this kind of culture is widespread (Prioli, 2008). A “multicontrol” approach, consisting of two reference sites and two possible impacted sites placed inside an

open sea farm, was adopted. Further five stations located at increasing distances from the edge of the culture up to 300 m along a transect following the main current direction were sampled to assess a possible impact gradient. Univariate biological indices and multivariate analysis revealed a certain fluctuation of benthic macrofaunal community during the overall sampling year mainly due to seasonality rather than the location of the sampling sites. The highest richness and density values recorded in spring, usually corresponding to the spawning and settlement phase of many benthic species in the Eastern Mediterranean (Gouvis et al., 1997), were mainly responsible for these seasonal differences. High spring densities observed everywhere, for example, were due to the great abundance of several species, especially C. equilibra. This amphipod is common in the whole area both on the natural sandy-mud seabed and on artificial constructions (aquaculture nets, floating buoys, ropes etc.) where it feeds directly on prey and organic particles captured from the water column (Fabi et al., 1998, 2002; Thiel et al., 2003). The summer collapse recorded for N, well evidenced by the strong reduction of C. equilibra, was likely induced by a dystrophic crisis caused by a decrease of oxygen close to the bottom (from mean value of 75% to 45%; Fabi et al., 2004) subsequent to water stratification. Such an oxygen depletion might have been a limiting factor for the survival of this and other species recruited in spring, also contributing to the simultaneous decrease of S and Sm at most of the investigated sites both inside and outside the farm (Sconfietti and Luparia, 1995).

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Fig. 6. Non-metric multi-dimensional scaling (MDS) plots in 2 dimensions for benthic macrofaunal data collected in each sampling season with superimposed clusters from Fig. 5, at similarity level of 84%, 74%, 75% and 79%. Abbreviations as in Figs. 1 and 5.

The effects induced by the dystrophic event persisted until winter when the recovery of some species was observed (Sm and J' significantly increased), although low densities were still recorded. Dystrophic deficiencies frequently occur during the summer along the coastal areas of the central and Northern Adriatic Sea where the wide availability of organic matter due to the river runoff, coupled with low water exchange and high temperatures may promote decreases of the dissolved oxygen concentration in the sediments with consequent collapse of the benthic macrofauna (Schinner et al., 1997; Crema et al., 1991; Marini et al., 2004). While isolation in lagoons, estuaries and sheltered waters limits the recovery of the invertebrate benthic assemblages after a dystrophic event (Sorokin et al., 1999; Ponti et al., 2007), in the present study the recovery was likely favoured by the open-sea location of the culture which usually ensures an adequate water renewal from fall to spring due to currents, waves and turbulent mixing by winds. However, independently from dystrophic events, high spring densities followed by an abrupt decrease in number of individuals occurring in summer has been reported by Gouvis et al. (1997) in the North Aegean Sea, as a result of the seasonal alternation in the dominance of certain species due to usual phenomena such as migration, predation and competition (Boesch et al., 1976; Little and Boyden, 1976; Thrush, 1999; Beukema et al., 2000). In terms of community species composition, the main contributors identified by SIMPER analysis for season and site groups did not highlight a real impact solely due to the farm, as many of them were common to most of sites and seasons. Some of these species are commonly known as indicators of organic enrichment, i.e. the deposit-feeder P. cirrifera, and the filter-feeders M. bidentata and C. gibba (Pearson and Rosemberg, 1978; Simboura and Zenetos, 2002; Bustos-Baez and Frid, 2003). The last one is also considered a pioneer species in recolonization of defaunated bottoms. Other taxa instead, such as O. fusiformis, show contradictory patterns, scoring positive in some studies (Pinedo et al., 1997; Elias et al., 2001) and negative in

others (Ambrogi et al., 1995; Nugues et al., 1996; Simboura and Zenetos, 2002; Bustos-Baez and Frid, 2003). O. fusiformis is a surfacedeposit feeder (Gambi, 1989) that alternates its feeding mechanism in relation with the environmental conditions. When high planktonic inputs are produced and flow conditions change, O. fusiformis can behave as a filter feeder (Gambi, 1989). However, the presence of species used as indicators of organic enrichment cannot be considered meaningful as a possible mussel farm impact in this case. In fact, they commonly occur with large abundances in the macrobenthic populations inhabiting the seabed of the North-Central Adriatic Sea between 12 and 15 m of depth. This coastal area, indeed, is frequently affected by physical disturbance (e.g. seasonally variable river discharges, anthropogenic eutrophication through excessive external nutrient input). As the time between subsequent disturbances is shorter than that required to complete the pattern of succession, a full recovery is usually not allowed and an intermittent one takes place with the occurrence of small, short-lived and opportunistic organisms (Crema et al., 1991; Fabi et al., 1998, 2002; Mistri, 2002). However, a more detailed analysis allowed us to identify a possible weak impact due to the farm. In fact, ANOSIM and SIMPER analysis pointed out a certain pattern Northwest-Southeast following the main current, with the highest dissimilarity between C and OT sites and the IN sites playing an intermediate role. This result was also confirmed by MDS and Cluster analysis which clearly separated C and OT sites in each season, while IN sites were always associated with one of the other two groups. The observed spatial pattern is related to the seasonal abundances and feeding habitat of most of the species recorded at the different site groups. Deposit-feeders (e.g. Prionospio spp.) were generally more abundant inside the farm and filter-feeders (e.g. C. gibba) at OT sites. Mussels, in fact, are extremely efficient filter-feeders and could compete for seston and phytoplankton with other species having the same feeding behaviour, whilst biodeposition of faecal matter

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from suspended mussels provides an additional food source for benthic deposit-feeders (Smith and Shackley, 2004). Moreover, the main current transported part of the organic wastes from the culture towards the Southeast inducing a greater occurrence of filter-feeders at OT sites in respect to C sites. The differences in the spatial distribution of these two trophic groups was more accentuated in summer in concomitance with a pool of factors such as low current intensity, water stratification and, finally, the mussel biomass inside the culture. In fall and winter the higher hydrodynamism due to currents and wave motion favoured the dispersion of faecal matter so leading to greater density homogeneity of the different species among all sites. However, a slight gradient of influence still remained in relation to re-suspension and/or export of mussel biodeposits extending up to 60 m SE from the culture in winter. The higher similarity found among all stations in spring (empty culture phase) in respect to the subsequent seasons (half-load phase and full-load phase) suggests an effect by the culture on the benthic assemblage during the mussels' active growth phases. The above results clearly indicate that open-sea mussel cultures have minimal detrimental effects on the benthic domain of the Western Adriatic coast where the local hydrographical features and the relatively high trophic conditions due to the great river runoff play a fundamental role in the dynamics of the biological components. The importance of farm location and hydrological conditions in the potential impact on the benthic biocenosis associated with mussel production (Hartstein and Rowden, 2004) is also confirmed with minimal impact at sites characterised by high hydrodynamic energy. The findings of this study largely agree with results achieved in the same area on biochemical, microbial and meiofaunal parameters (Danovaro et al., 2004) as well as with studies performed in other countries, such as Southwest Ireland (Chamberlain et al., 2001), Tasmania, Australia, (Crawford et al., 2003) and Southeast Brazil (da Costa and Nalesso, 2006), showing minimal mussel farming effects. At present, mussel farming together with Japanese carpet shell (Tapes philippinarum) culture in lagoons, represent the main aquaculture activities in Italy. Mussel cultures, initially placed in lagoons and sheltered bays, have been extended in the last 10 years to opensea areas where there are more suitable environmental conditions and greater space availability. The increasing demand for new cultures, especially along the Western coast of the Adriatic Sea, has lead some local authorities to identify specific marine farming zones in order to avoid conflicts with other users of the coastal areas. These zones are assessed for their suitability for marine farming (e.g. suitable depth, habitat type, water quality, distance from the harbours and trade routes, etc.), but no environmental controls are required after the building of the cultures. This study, conducted 6/7 years after the installation of the mussel farm, has shown that shellfish culture along the Italian Adriatic coast has little impact on the benthic ecosystem. It agrees with the findings of Danovaro et al. (2004) in a simultaneous work on meiofauna carried out in the same area. Despite one-year of data might not be sufficient to completely assess the effects of shellfish farming on ambient ecosystem due to inter-annual variability of environmental conditions, these results represent a baseline to set up long-term monitoring and develop management plans to ensure the sustainability of shellfish culture in shallow coastal waters. Monitoring programs integrated with pre-surveys would be recommended especially in areas intensively exploited by mussel farming. Acknowledgements The Authors wish to thank MIPAF (Ministero per le Politiche Agricole e Forestali, Italy) who financially supported the study. Many thanks also to the crew of the R/V Tecnopesca II of CNR-ISMAR who actively participated in the sampling at sea and the Cooperativa Mare of Cattolica for their great logistic contribution.

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