© 2006 International Council for the Exploration of the Sea
The infaunal community in experimentally seeded low and high density Manila clam (Tapes philippinarum) beds in a Po River Delta lagoon (Italy)
Department of Biology, University of Ferrara Via L. Borsari 46, 44100 Ferrara, Italy
*Correspondence to S. Mantovani: tel: +39 532 291737; fax: +39 532 249761. e-mail: mntsra{at}unife.it.
The Sacca di Goro is a shallow, brackish, eutrophic coastal lagoon in the southernmost part of the Po River Delta (northern Adriatic Sea, Italy). It is heavily exploited for rearing the Manila clam (Tapes philippinarum), mean annual production since 1986 being 10 000 t. Commercial cultivation of bivalves can exert severe impact on a local environment, especially on the invertebrate community, reducing species richness and abundance. An in situ experiment was conducted from March 2003 to February 2004 to examine the effect of clam cultivation on the macrobenthic community. Replicated sites within an area licensed for clam farming were seeded with low (500 m–2) and high (1500 m–2) clam densities; the surrounding unseeded areas were used as a control. There were only weak effects of clam presence and density on macrobenthic community abundance and functional group composition. The main determinants regulating the macrobenthic community were seasonal variations in other biota, particularly proliferation of the invasive mussel, Musculista senhousia, in August, which in turn caused a significant increase in the biomass of surface deposit-feeders and the subsequent development of Ulva rigida beds in September.
Keywords: clam cultivation, clam seeding, eutrophic lagoon, macrobenthos
Received 12 April 2005; accepted 12 February 2006.
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Introduction |
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There has been increasing recent interest in evaluating the collateral effects of commercial cultivation of bivalves on the local marine environment (Sorokin et al., 1999; Bartoli et al., 2001; Jie et al., 2001; Dame et al., 2002), especially on macrobenthic communities (Kaiser et al., 1996; Drake and Arias, 1997; Spencer et al., 1997; Gaspar et al., 2002, 2003). The main effect on non-target species is a reduction in species richness and abundance (Commito, 1987; Dittman, 1990; Guenther, 1996; Ragnarsson and Raffaelli, 1999; Beadman et al., 2004; Pranovi et al., 2004), although in some cases the opposite effect has been recorded. This was caused by the use of plastic nets to protect clams from predation by shorebirds and crabs (Spencer et al., 1992), which increased sedimentation rates and consequently the density of some species of infaunal deposit-feeding worms (Spencer et al., 1997).
This study was carried out in the Sacca di Goro, a shallow, brackish, eutrophic coastal lagoon located in the southernmost part of the Po River Delta (northern Adriatic Sea, Italy); the surface area is some 26 km2 and the average depth 1.5 m. The lagoon receives freshwater input rich in organic and mineral nutrients, derived from urban effluents and agricultural run-off. These factors are responsible for important alterations in ecosystem functioning characterized by eutrophic and dystrophic conditions in summer, algal blooms, oxygen depletion, and hydrogen sulphide production (Giordani et al., 1997; Viaroli et al., 2001). Clam farming has been practiced continuously in the lagoon since 1986 (Carrieri et al., 1992), and the mean annual yield has been 10 000 t. Clams are cultivated in licensed areas covering approximately 9 km2 of the lagoon surface. Approximately 1.5–2 km2 are intensively cultivated at a density of >500 m–2 (Rossi, 2000).
The aim of this study was to investigate the effect of rearing clams, at low and high stocking densities, on the macrobenthic community, and on the taxonomic and functional composition of the community throughout an annual cycle, from seeding to harvesting.
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Material and methods |
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Study area
The experiment was carried out for 11 months, starting on 12 March 2003 (the preferred seeding month) and ending on 12 February 2004, within an area licensed for clam farming (Figure 1) in the Sacca di Goro. The experimental area was selected with regard to sandy/silty sediment characteristics, linked to a hydrodynamic regime that allows optimal clam growth and survival (Rossi, 2000). Before seeding, existing clams were removed from the experimental site by professional fishers.
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The study area (400 m2) was divided into subunits (Figure 2), left (Le) and right (R), seeded with clams of average length 19 ± 2 mm and weight 1.65 ± 0.51 g, at low (L) 500 m–2 and high (H) 1500 m–2 densities, for four treatments, respectively, labelled LLe, HLe, LR, and HR. The experimental area that remained unseeded served as a control (CR and CLe).
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Clam sampling and analysis
Samples were collected monthly in each of the four cultivated sites from 12 March 2003 to 12 February 2004. Triplicate samples were taken randomly using two square frames, 40 cm side for the 500-m–2 density seeding, and 20 cm side for the 1500-m–2 density seeding, designed to allow collection of adequate sample sizes, based on a pilot survey (data not shown). The sediment inside the frame was collected to a depth of 25 cm, and the samples were washed through a net (5-mm mesh) to remove the clams. These were transferred quickly to the laboratory where individual lengths and weights were measured.
Macrobenthic community sampling and analysis
Triplicate samples were collected with a van Veen grab (area 0.06 m2) with a penetration depth of 12 cm (approximately 10 cm at the edge) at each site in March, April, June, August, and September, when macroalgal blooms and related dystrophic events were likely, and in February, after winter. Samples were filtered rapidly through a sieve of 0.5-mm mesh, and the material retained was fixed in 8% buffered formalin and stained with Rose Bengal to facilitate sorting and identification. Each item was identified to species level when possible, using standard reference texts. The numbers of each taxon were recorded. The functional group for each taxon was defined, and the biomass was determined as ash-free dry weight (dw), after drying at 100°C for 24 h and burning at 450°C for 5 h.
When present in the sample, the macroalga Ulva rigida was separated from the sediment, and its biomass determined as dry weight, after drying at 100°C for 24 h.
Data analysis
Macroinvertebrate community structure was assessed on the basis of abundance, biomass, species richness (Margalef's d index), diversity (Shannon's H index), evenness (Pielou's J index), and functional group composition. Differences between L and H density and control sites, i.e. the effect of the factors "site" and "density", or between the sampling dates (factor "month"), considering separately macrofauna, and clam length and weight, were tested with MANOVA. Normality of data was assumed, and homoscedasticity was tested using Cochran's test. Post-hoc comparisons were performed using a Tukey test.
The overall percentage contribution of each species to the average dissimilarity between "densities" and "times" was ascertained using SIMPER (PRIMER ecological statistical software package; Clarke and Warwick, 1994).
To analyse benthic communities, clams were removed, because they were sampled and analysed separately.
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Results |
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Manila clams
The Manila clam seeding densities of 500 and 1500 m–2 remained constant throughout the study period. Clams grew exponentially, reaching commercial size (D.P.R. 1639/68, Marine Fisheries Law) in October, at average lengths of 35.4 and 36.4 mm, corresponding to average weights of 10.54 and 12.15 g, respectively, at H and L densities.
Macrozoobenthic community
The statistical analysis of macrozoobenthic community data (abundance, biomass, richness, diversity, evenness, and functional groups) revealed no significant effect (F1,5 = 1.421; p > 0.05) of the factor "site", i.e. there were no differences between Le and R, L and H density, and control, so the data from replicated sites were pooled. Consequently, results are presented as the average of six replicates for each site (L, H, and C) for density and month, for the parameters listed above.
The macrozoobenthic species list, compiled over all sampling periods, consisted of 28 taxa (Table 1). Variations in total abundance (Figure 3) were not significantly different (F2,90 = 1.626; p > 0.05) in the cultivated sites or control, except in August, when the control (25 782 m–2) and H density (22 804 m–2) experienced a reduction (F5,90 = 5.717; p < 0.01) not found at the L-density sites. In September all plots contained lower densities than in June (F5,90 = 6.012; p < 0.01) and February (F5,90 = 5.199; p < 0.01).
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The biomass data followed the same pattern of no significant difference between sites (F2,90 = 1.849; p > 0.05), with the lowest value in September (F5,90 = 7.187; p < 0.01), but complete recovery in February (F5,90 = 9.159; p < 0.01).
SIMPER showed that the dominant taxa (90% of total abundance) in all treatments throughout the study period were the polychaetes Polydora ciliata, Capitella capitata, Prionospio multibranchiata, and Streblospio shrubsolii, together with the amphipods Microdeutopus gryllotalpa and Ampelisca sp., showing average dissimilarities never higher than 40%. SIMPER also revealed a trend of increasing complexity, as four species (S. shrubsolii, P. multibranchiata, C. capitata, and N. succinea) contributed 90% of the similarity in March. These four species increased to five in April, six in June, and seven in August and September, in relation to the successive appearance of the amphipods Ampelisca sp., M. gryllotalpa, and Gammarus spp., respectively.
Community indices are reported in Table 2. Shannon's index increased significantly (F5,90 = 23.894; p < 0.01) from March to June, decreased in August (F5,90 = 18.544; p < 0.01) in H and C, and increased (F5,90 = 9.111; p < 0.01) in February 2004, in all treatments. A parallel trend was revealed for Pielou's index, with the lowest values in August (F5,90 = 12.170; p < 0.01) in H and C. Margalef's index increased (F5,90 = 23.709; p < 0.01) over the sampling period.
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Functional group composition indicated a strong dominance of surface deposit-feeders (SDF), mainly S. shrubsolii and P. multibranchiata (Figure 4). The density of SDF showed a parallel trend in H and L density, and C, in all months except August, when L (36 710 m–2) was significantly higher (F2,90 = 3.299; p > 0.05) than H (16 403 m–2) and C (19 209 m–2). Subsurface deposit-feeders (SSDF) remained stable throughout the study period, densities ranging from 700 to 2000 m–2, but increased significantly (F5,90 = 3.614; p < 0.05) in February (4174, 7689, and 7634 m–2). Filter-feeders (FF) were present at densities <200 m–2. They peaked in August (F5,90 = 40.429; p < 0.01), reaching densities of 4865, 4637, and 5260 m–2, in H, L, and C, respectively, and decreased (F5,90 = 31.981; p < 0.01) in September (600–2000 m–2) and February (900–1500 m–2). Further, the mussel Musculista senhousia, rarely found from March to June (0–60 m–2), built extended mats in H- (3688 m–2) and L-density (4643 m–2) cultivated sites, and in C (3928 m–2) during August.
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Ulva rigida biomass
Ulva rigida was observed in the experimental area in August (Figure 5), in the sites with H density first, with a biomass of 52 and 20 g dw m–2, respectively, for HLe and HR. In September the macroalgal bed completely covered the area, with a biomass varying from 31 (in HR) to 364 g dw m–2 (in LR). In February, the experimental area was completely devoid of algae.
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Discussion |
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Invertebrate abundance in temperate soft-bottom habitats usually varies seasonally, with two peaks typically in spring and autumn (Guelorget and Michel, 1979; Castel et al., 1989; Arias and Drake, 1994). In the Sacca di Goro lagoon, such temporal fluctuation was constantly disturbed by clam rearing, because the licensed areas cover >30% of the surface and the remaining part is variably exposed to some activity, such as harvesting naturally settled adult clams and/or spat.
In common with other coastal habitats subjected to heavy fishing stress (Auster et al., 1996; Frid et al., 1996; Jennings and Kaiser, 1998), it is difficult to identify control sites where the benthic community is undisturbed. Consequently, in the present study, the control site selected was an area not recently affected by clam farming, but potentially indirectly affected by disturbance in nearby parts of the lagoon. A previous study on the effects of manual harvesting on a clam-cultivation area of the Sacca di Goro lagoon showed recovery within a month of harvesting (Castaldelli et al., 2003). Therefore, as the control site had not been exposed to direct anthropogenic disturbance for a year prior to the experiment (March 2003), the resident macrobenthic community was considered to be undisturbed.
Previous studies on the effects of bivalve cultivation on non-target species identified significant alteration of community structure, in the form of reduced diversity and richness (Commito, 1987; Dittman, 1990; Guenther, 1996; Ragnarsson and Raffaelli, 1999; Beadman et al., 2004; Pranovi et al., 2004), or more specific effects on particular taxa, principally on burrow-dwelling invertebrates (Flach, 1996; Spencer et al., 1996). The main causes of these changes are ascribable to the presence of unstable sediments, common in bivalve cultivation areas, owing to the high rates of deposition of faeces and pseudo-faeces, movement of bivalves (Kautsky and Evans, 1987), and the lack of space for burrow construction (Jensen and Kirstensen, 1990).
In this study, significant differences in density, biomass, and functional group composition were found rarely between treatments and control. The macrozoobenthic community appeared to be dominated by highly tolerant opportunistic species of small size, high motility, and short life cycle, as reported by Mistri et al. (2001) for locations of the Sacca di Goro outside the licensed clam-cultivation areas, and in other European lagoons and embayments subjected to trawling and mollusc-farming (Drake and Arias, 1997; Mistri et al., 2000; Thrush et al., 2001). In our experimental site, small polychaetes (<3 mm long) dominated, in both cultivated and control areas, indicating the absence of spatial limitation of clams evident in other environments (Jensen and Kirstensen, 1990).
Clam presence and density seemingly did not affect the temporal fluctuation of invertebrate abundance and functional group composition, in apparent contrast to studies conducted in the United Kingdom (Kaiser et al., 1996; Spencer et al., 1996, 1997), where plastic nets, protecting clams from crabs and shorebirds, enhanced sedimentation rates and deposit-feeder densities (Spencer et al., 1992). Other bivalve cultivation techniques, such as American hard-shell clams (Mercenaria mercenaria) being placed in net bags on intertidal shores (Mojica and Nelson, 1993), or mussels (Mytilus galloprovincialis), suspended in large-mesh plastic sacks (Nizzoli et al., 2005), increase accumulation of particulate organic matter in the sediment, resulting in reduced diversity of natural macrofaunal assemblages, and favouring the dominance of small, hypoxia–anoxia tolerant, species (Haven and Morales-Alamo, 1966; Dame et al., 1980). Nets are not necessary in the subtidal, naturally sheltered, clam-farming areas in the Sacca di Goro, and marine vivification was recently increased by dredging many channels adjacent to rearing sites, favouring the flushing of faeces and pseudo-faeces from the area.
The potential effect of organic matter accumulation became evident during the rapid increase of filter-feeders recorded in August (Figure 4), owing to the presence of the mussel Musculista senhousia, which did not affect our experiment, i.e. clam densities altering clam growth and/or mortality (Mistri, 2004). Extended mats of M. senhousia retained more organic matter on the sediment, and this modified the benthic community composition, favouring detritivores such as S. shrubsolii, as already reported (Crooks, 2001; Mistri, 2003). One of the highest SDF abundances (36 710 m–2, mainly S. shrubsolii and P. multibranchiata) was recorded in the L-density site, concomitant with the highest M. senhousia abundance (4643 m–2).
In the same period, there was a significant decrease of SDF and an increase of amphipods (M. gryllotalpa and Gammarus spp.) in plots H and C, in relation to the appearance (August) and development (September), of the macroalga U. rigida, reducing also the abundance of M. senhousia (F5,90 = 36.429; p < 0.01). Surface deposit-feeders are the group that is most sensitive to the presence of macroalgal beds, being negatively affected by the reduction of oxygen related to algal respiration and enhanced bacterial activity (Norkko and Bondsdorff, 1996; Osterling and Pihl, 2001).
A study conducted in other areas of the Sacca di Goro lagoon failed to show significant correlations between Gracilaria verrucosa biomass and macroinvertebrate community parameters. Dystrophic events were not recorded, and the only negative effect was on the dominant bivalve species, Cerastoderma glaucum, which suffered from physical interference with filter-feeding activity, as hypothesized by Mistri et al. (2001). In the licensed clam-farming areas, G. verrucosa thalli were rarely found, while Ulva spp. accumulation, decomposition, and related dystrophic crises took place for many years (Viaroli et al., 1992, 2001, 2003), leading to mass mortality of clams and non-target benthic fauna (Rossi, 2000).
At the experimental site, rapid development of U. rigida and its crash at the end of summer appeared to be the strongest disturbance, indicating that August and September were the most dominant months for this alga, as confirmed by diversity and evenness values which were lower than those registered after the cold season (February).
The benthic community in clam-culture areas of the Sacca di Goro lagoon presented a characteristic composition and structure, established by a 20-year chronic regime of anthropogenic disturbance, owing to both eutrophication-related phenomena and clam-rearing practices. In the present situation, sudden and unpredictable events, such as the rapid development and disappearance of M. senhousia and U. rigida at the end of summer, appeared much more influential in regulating macrofaunal assemblages within clam-cultivation sites, than the clams.
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Acknowledgements |
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We thank the Fishermen's Cooperative of Goro, Italy, who kindly allowed the experimentation within its clam farm. We also thank Edoardo Turolla who contributed clam sampling and analysis. This study is part of the project "Effetti della molluschicoltura sul riciclo dei nutrienti in lagune costiere distrofiche: strategie di gestione a basso impatto ambientale per gli allevamenti di vongole e il controllo delle fioriture algali" supported by MiPAF, the Italian Ministry for Agricultural and Forest Policies, VI Triennial Programme for Fishery and Aquaculture.
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References |
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Arias A.M. and Drake P. (1994) Structure and production of the benthic macroinvertebrate community in a shallow lagoon in the Bay of Cadiz. Marine Ecology Progress Series 115:151–167.[Web of Science]
Auster J.R., Malatesta R.J., Langton R.W., Watling L., Valentine P.C., Donaldson C.L.S., Langton E.W., Shepard A.N., Babb I.G. (1996) The impacts of mobile fishing gear on seafloor habitats in the Gulf of Maine (Northwest Atlantic): implications for the conservation of fish populations. Reviews in Fisheries Science 4:185–202.
Bartoli M., Nizzoli D., Viaroli P., Turolla E., Castadelli G., Fano E.A., Rossi R. (2001) Impact of Tapes philippinarum farming on nutrient dynamics and benthic respiration in the Sacca di Goro. Hydrobiologia 455:203–212.[CrossRef][Web of Science]
Beadman H.A., Kaiser M.J., Galandi M., Shucksmith R., Willows R.I. (2004) Changes in species richness with stocking density of marine bivalves. Journal of Applied Ecology 41:464–475.[CrossRef][Web of Science]
Carrieri A., Paesanti F., Rossi R. (1992) Risultati dell'introduzione di vongola filippina, Tapes philippinarum (Adams & Reeve, 1850) nella Sacca di Goro (Delta del Po). Oebalia 17:297–104.
Castaldelli G., Mantovani S., Welsh D.T., Rossi R., Mistri M., Fano E.A. (2003) Impact of commercial clam harvesting on water column and sediment physicochemical characteristics and macrobenthic community structure in a lagoon (Sacca di Goro) of the Po River delta. Chemistry and Ecology 19:161–171.[CrossRef]
Castel J., Labourg J.P., Escaravage V., Auby I., Garcia M.E. (1989) Influence of seagrass beds and oyster parks on the abundance and biomass pattern of meio- and macrobenthos in tidal flats. Estuarine, Coastal and Shelf Science 28:71–85.[CrossRef]
Clarke K.R. and Warwick R.M. (1994) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation(Natural Environment Research Council, UK) 144 pp.
Commito J.A. (1987) Adult–larval interactions: predictions, mussels and cocoons. Estuarine, Coastal and Shelf Science 25:599–606.[CrossRef]
Crooks J.A. (2001) Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon. Biological Invasions 3:23–36.[CrossRef]
Dame R., Bushek D., Allen D., Lewitus A., Edwards D., Koepfler E., Gregory L. (2002) Ecosystem response to bivalve density reduction: management implications. Aquatic Ecology 36:51–65.[CrossRef]
Dame R., Zingmark R., Stevenson H., Nelson D. (1980) Filter feeding coupling between the estuarine water column and benthic subsystem. In Kennedy V.S. (Ed.). Estuarine Perspectives(Academic Press, New York) pp. 521–526.
Dittman S. (1990) Mussel beds – amensalism or amelioration for intertidal fauna? Helgoland Marine Research 44:335–352.
Drake P. and Arias A.M. (1997) The effect of aquaculture practices on the benthic macroinvertebrate community of a lagoon system in the Bay of Cadiz (Southern Spain). Estuaries 20:677–688.[CrossRef][Web of Science]
Flach E.C. (1996) The influence of the cockle, Cerastoderma edule, on the macrozoobenthic community of tidal flats in the Wadden Sea. Marine Ecology 17:87–98.
Frid C.L.J., Buchanan J.B., Garwood P.R. (1996) Variability and stability in benthos: twenty-two years of monitoring of Northumberland. ICES Journal of Marine Science 53:978–980.
Gaspar M.B., Leitão F., Santos M.N., Chícharo L., Dias M.D., Chícharo A., Monteiro C.C. (2003) A comparison of direct macrofaunal mortality using three types of clam dredges. ICES Journal of Marine Science 60:733–742.
Gaspar M.B., Leitão F., Santos M.N., Sobral M., Chícharo L., Chícharo A., Monteiro C.C. (2002) Influence of mesh size and tooth spacing on the proportion of damaged organisms in the catches of the Portuguese clam dredge fishery. ICES Journal of Marine Science 59:1228–1236.
Giordani G., Azioni R., Batoli M., Viaroli P. (1997) Seasonal variations of sulphate reduction rates, sulphur pools and iron availability in the sediment of a dystrophic lagoon (Sacca di Goro, Italy). Water Air and Soil Pollution 99:363–371.
Guelorget O. and Michel P. (1979) Les peuplements benthiques d'un étang littoral languedocien, l'étang du Prevost (Hérault). 1. Etude quantitative de la macrofaune des vases. Téthys 9:49–64.
Guenther C.P. (1996) Development of small Mytilus beds and its effect on resident intertidal macrofauna. Marine Ecology 17:117–130.
Haven D.S. and Morales-Alamo R. (1966) Aspects of biodeposition by oysters and other invertebrate filter-feeders. Limnology and Oceanography 11:487–498.[Web of Science]
Jennings S. and Kaiser M.J. (1998) The effect of fishing on marine ecosystems. Advances in Marine Biology 34:201–351.[Web of Science]
Jensen K.T. and Kirstensen L.D. (1990) A field experiment on competition between Corophium volutator (Pallas) and Corophium arenarium (Crawford) (Crustacea: Amphipodia): effects on survival, reproduction and recruitment. Journal of Experimental Marine Biology and Ecology 137:1–24.[CrossRef][Web of Science]
Jie H., Zhinan Z., Zishan Y., Widdows J. (2001) Differences in the benthic–pelagic particle flux (biodeposition and sediment erosion) at intertidal sites with and without clam (Ruditapes philippinarum) cultivation in eastern China. Journal of Experimental Marine Biology and Ecology 261:245–261.[CrossRef][Web of Science][Medline]
Kaiser M.J., Edwards D.B., Spencer B.E. (1996) Infaunal community changes as a result of commercial clam cultivation and harvesting. Aquatic Living Resources 9:57–63.[CrossRef][Web of Science]
Kautsky N. and Evans S. (1987) Role of biodepuration by Mytilus edulis in the circulation of matter and nutrients in a Baltic coastal system. Marine Ecology Progress Series 38:201–212.[Web of Science]
Mistri M. (2003) The non-indigenous mussel Musculista senhousia in an Adriatic lagoon: effects on benthic community over a ten year period. Journal of the Marine Biological Association of the United Kingdom 83:1277–1278.[CrossRef][Web of Science]
Mistri M. (2004) Effect of Musculista senhousia mats on clam mortality and growth: much ado about nothing? Aquaculture 241:207–218.[CrossRef][Web of Science]
Mistri M., Fano E.A., Rossi G., Caselli K., Rossi R. (2000) Variability in macrobenthos communities in the Valli di Comacchio, northern Italy, an hypereutrophized lagoonal ecosystem. Estuarine, Coastal and Shelf Science 51:599–611.[CrossRef]
Mistri M., Rossi R., Fano E.A. (2001) Structure and secondary production of a soft bottom macrobenthic community in a brackish lagoon (Sacca di Goro, north-eastern Italy). Estuarine, Coastal and Shelf Science 52:605–616.[CrossRef]
Mojica R. and Nelson W.G. (1993) Environmental effects of hard clam (Mercenaria mercenaria) aquaculture in the Indian River Lagoon, Florida. Aquaculture 113:313–329.[CrossRef][Web of Science]
Nizzoli D., Welsh D.T., Bartoli M., Viaroli P. (2005) Impacts of mussel (Mytilus galloprovincialis) farming on oxygen consumption and nutrient recycling in a eutrophic coastal lagoon. Hydrobiologia 550:183–198.[CrossRef][Web of Science]
Norkko A. and Bondsdorff E. (1996) Population responses of coastal zoobenthos to stress induced by drifting algal mats. Marine Ecology Progress Series 140:141–151.[Web of Science]
Osterling M. and Pihl L. (2001) Effects of filamentous green algal mats on benthic macrofaunal functional feeding groups. Journal of Experimental Marine Biology and Ecology 236:159–183.
Pranovi F., Da Ponte F., Raicevich S., Giovanardi O. (2004) A multidisciplinary study of the immediate effects of mechanical clam harvesting in the Venice Lagoon. ICES Journal of Marine Science 61:43–52.[CrossRef][Web of Science]
Ragnarsson S.A. and Raffaelli D. (1999) Effects of the mussel Mytilus edulis on the invertebrate fauna of sediments. Journal of Experimental Marine Biology and Ecology 241:31–43.[CrossRef][Web of Science]
Rossi R. (2000) Gestione produttiva della Sacca di Goro (Delta del Po): analisi dei parametri ambientali, biologici e socioeconomici per la valutazione del regime concessorio. Ministero per le Politiche Agricole e Forestali, quinto piano triennale. 28 pp.
Sorokin I.I., Giovanardi O., Pranovi F., Sorokin P.I. (1999) Need for restricting bivalve culture in the southern basin of the Lagoon of Venice. Hydrobiologia 400:141–148.[CrossRef][Web of Science]
Spencer B.E., Edwards D.B., Millican P.F. (1992) Protecting Manila clam (Tapes philippinarum) beds with plastic netting. Aquaculture 105:251–268.[CrossRef][Web of Science]
Spencer B.E., Kaiser M.J., Edwards D.B. (1996) The effect of Manila clam cultivation on an intertidal benthic community: the early cultivational phase. Aquaculture Research 27:261–276.
Spencer B.E., Kaiser M.J., Edwards D.B. (1997) Ecological effects of intertidal Manila clam cultivation: observations at the end of the cultivation phase. Journal of Applied Ecology 34:444–452.[CrossRef][Web of Science]
Thrush S.F., Hewitt J.E., Funnel G.A., Cummings V.J., Ellis J., Schultz D., Talley D., Norkko A. (2001) Fishing disturbance and marine biodiversity: role of habitat structure in simple soft-sediment systems. Marine Ecology Progress Series 221:255–264.[Web of Science]
Viaroli P., Azzoni R., Bartoli M., Giordani G., Tajé L. (2001) Evolution of the trophic conditions and dystrophic outbreaks in the Sacca di Goro lagoon (northern Adriatic Sea). In Faranda F.M., Guglielmo L., Spezie G. (Eds.). Structure and Processes in Mediterranean Ecosystems(Springer, Berlin) pp. 467–475.
Viaroli P., Batoli M., Giordani G., Azioni R., Zizzoli D. (2003) Short term changes of benthic fluxes and oxygen depletion risk in a coastal lagoon with clam farming (Sacca di Goro, Po River Delta). Chemistry and Ecology 19:173–187.[CrossRef]
Viaroli P., Pugnetti A., Ferrari I. (1992) Ulva rigida growth and decomposition processes and related effects on nitrogen and phosphorus cycles in a coastal lagoon (Sacca di Goro, Po River Delta). In Colombo G., Ferrari I., Ceccherelli V.U., Rossi R. (Eds.). Marine Eutrophication and Population Dynamics, Proceedings of the 25th EMBS(Olsen & Olsen, Fredensborg, Denmark) pp. 77–84.
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