Tin free antifouling paints as potential contamination source of metals in sediments and gastropods of the southern Venice lagoon

Continental Shelf Research 45 (2012) 34–41

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Research papers

Tin free antifouling paints as potential contamination source of metals in sediments and gastropods of the southern Venice lagoon Daniela Berto a,n, Rossella Boscolo Brusa a, Federica Cacciatore a, Stefano Covelli b, Federico Rampazzo a, Otello Giovanardi a, Michele Giani c a

Istituto Superiore per la Protezione e la Ricerca Ambientale, Brondolo, 30015 Chioggia, Italy Dipartimento di Matematica e Geoscienze, Via Weiss 2, 34128 Trieste, Italy c Istituto Nazionale di Oceanografia e Geofisica Sperimentale, 34151 Trieste, Italy b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 September 2011 Received in revised form 21 May 2012 Accepted 28 May 2012 Available online 7 June 2012

The southern Venice lagoon has been affected by an increase of several anthropogenic activities (dockyards, harbours and marina) which have contributed to enrich sediments with metals in the recent years. The contamination of metals in the surface sediments along with their accumulation in the gastropod Nassarius reticulatus were investigated. Highest metal concentrations of Cu, Zn, Pb and Cr found in the dockyards and marina sites suggest their possible past and recent use as biocides in the antifouling paints. The enrichment factor (EF) showed highest values (EF4 10) near the dockyards, harbour and marina sediments for Cu, where the use of the antifouling tin free paints has been more relevant. High levels of metals were also found in the target gastropods. Biota-Sediment-AccumulationFactor and correlation analyses pointed out a significant mobilization of metals, particularly Cu, from sediments and their accumulation in the gastropods. & 2012 Elsevier Ltd. All rights reserved.

Keywords: Antifouling paints Gastropods Nassarius reticulatus Accumulation factor Venice lagoon Metals

1. Introduction Anthropogenic heavy metals have been introduced into the aquatic environment directly by industrial activities, sewage treatments, urban discharges, atmospheric depositions and also by the use of biocides in anti-fouling paints on ship hulls. Chemicals, including organo-mercury (Hg) compounds, lead (Pb), arsenic (As) and DDT, were historically used as biocides in antifouling paints (Yebra et al., 2004). However, such compounds pose severe environmental and human health risk, and they were voluntarily withdrawn by the paint industry during the early 1960s (Bennett, 1996). They were largely replaced by tributyltin (TBT) compounds (Hoch, 2001). Considering the high toxicity of TBT-based antifouling paints, their use was banned since 2003 and phased out on all vessels since 2008 (Reg. EC 782/2003). The concern over the harmful side effects of TBT on the aquatic environment has resulted in significant development of TBT-free systems (Evans et al., 2000; Yebra et al., 2004) resulting in the reuse of other metal based antifouling paints, like copper (Cu)based paints (Yebra et al., 2004 and authors therein). Copper oxide is the most used biocide in the composition of these

n

Corresponding author. E-mail address: [email protected] (D. Berto).

0278-4343/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.csr.2012.05.017

paints (Boxall et al., 2000; Schiff et al., 2004) but zinc (Zn)-based antifouling compounds are also used (Yebra et al., 2004 and therein authors). A list of the most commonly used nontoxic pigments in ship bottom paints as zinc oxide, zinc dust, iron oxides, silica, and magnesium silicate were reported by ADAMSON (1922, 1937). Moreover the Zn compounds are more frequently a part of the anticorrosive, but may also be used in the antifouling coatings. With regard to the soluble pigment Zn(II) oxide, there is a total lack of studies on its behaviour in sea water (e.g. dissolution rate) and its consequent effect on antifouling paint whereas its use as sacrificial anode on boat motors is well known. In addition to these, pigments such as chrome green, chrome yellow, and various lakes may be used for inert and colouring purposes in association with organotins polymers and antifouling paints Turner et al., 2009). Lead finds its way into the aquatic environment via atmospheric inputs as well as from leaded gas leaking from boats (Pb was not phased out of use in boats until the late 1980s). Several works described the sediment contamination by metals in the northern and central Venice lagoon (e.g. Bellucci et al., 2002; Pavoni et al., 1992) but a few studies addressed to the southern area (Berto et al., 2006, 2007). The intense ship traffic (1.106 t y  1) due to the presence of the Chioggia harbour, small ferries and the presence of many marinas, dockyards and

D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

shipyards added with the most important fishing fleet (APAT, 2005) of northern Adriatic sea contribute to increase the potential risk of contamination in the surface sediments of this area in the last decades. Harvesting of Manila clam (Tapes philippinarum) by mean of specific gears is an important cause of resuspension of bottom sediments (Pranovi et al., 2004) causing erosion in the central lagoon with a global sediment loss of ca. 1.2 million tonnes year  1 (Sfriso et al., 2005). More recently, in order to create a new commercial harbour in the Chioggia area, intense dredging has become a very common activity causing relevant sediment resuspension which can be responsible for metals release from sediments into the water column. However, the knowledge of the distribution of heavy metals in sediments does not allow determining the real extent of their bioavailability and, consequently, the toxicity and risk of their accumulation into the aquatic trophic chain (Blackmore, 1998). Different organisms and species show different response mechanisms to metal ions and organisms which accumulate metals in their tissues and may therefore be analyzed as a measure of bioavailability of metals in the habitat (Rainbow, 1995). Circumstantial evidences indicated that concentrations of several metals (e.g. Cd, As, Cr, and Zn) in marine gastropods can be higher than concentrations measured in marine bivalves that are frequently consumed by predatory gastropods (Wang and Ke, 2002). The netted dog whelk Nassarius reticulatus (Linnaeus, 1758), scavenger and carrion feeder, dwelling on any type of bottom sediments at water depths of 0–20 m (de Kluijver et al., 2000), could be used for biomonitoring coastal contamination due to its capacity in accumulating heavy metals (Kaland et al., 1992). The distribution area of this snail extends in the Atlantic Ocean from Norway to Morocco. This species lives in the North Sea, the Kattegat and western Baltic Sea, Black Sea and Mediterranean Sea (e.g., de Kluijver et al., 2000) and it has been used in TBT monitoring programmes throughout Europe (Barreiro et al., 2001; Barroso et al., 2000; Berto et al., 2007; Couceiro et al. 2009) as well as in biomonitoring metal contamination, especially mercury (Berto et al., 2006; Coelho et al., 2006). This study aimed at assessing the contamination of metals (specifically Cu, Cr, Zn and Pb), potentially introduced via anthropogenic inputs, in the surface sediments of the southern Venice Lagoon and their bioaccumulation in gastropods N. reticulatus, in order to understand whether the relevant use of marine antifouling tin-free biocide-based products has contributed to increase metals abundance contents in this lagoon environment.

2. Materials and methods 2.1. Study area The Venice lagoon (Northern Adriatic Sea, Italy) is a transitional coastal environment covering a surface area of 549 km2 and it is characterized by a network of channels of various depths, estuaries, salt marshes and mudflats; the mean water depth is about 0.6 m, and the tidal range is less than 1 m. Three inlets connect the lagoon with the open sea (Lido, Malamocco and Chioggia, from north to south with mean depth 14, 17 and 8 m respectively). Major man-made transformations have especially taken place since the 1940: large chemical and metallurgic industrial plants were established at the edge of the lagoon (the Porto Marghera industrial district); a deep canal (Canale dei Petroli) was dug across the lagoon to serve the industrial district. The study area is located in the southern basin of the Venice lagoon, near the town of Chioggia (53,470 inhabitants, Fig. 1), affected by a constant increase in dockyards, harbours, marinas and shipping activities in the recent years. Moreover, the central

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and southern lagoons have been deeply affected by Manila clams harvesting since the end of the 1980, based on mechanical techniques that cause resuspension and mixing of surface sediments down to several centimetres depth. This activity along with dredging operations recently performed in the southern basin of the Venice lagoon may have largely made possible diffusion of contaminants. 2.2. Sampling Samples were collected in the southern Venice lagoon and in coastal area of Adriatic Sea from April to September 2003. Sampling sites were distinguished as Dockyards, Harbours, Marina, Urban area, Lagoon channels and Sea-coastal area on the basis of their location and human activities involved (Fig. 1). Sediments were sampled by an Ekman grab at 34 sites. The upper 2–3 cm were recovered and collected into acid-cleaned glass containers, rapidly homogenized, sieved through 200 mm nylon net and kept at –20 1C until analysis. Pools of 20–40 specimens of netted dog whelk, N. reticulatus were caught by a wire basket at 11 of the 36 sites where sediments were sampled. The mean shell length and width of all the collected specimens of N. reticulatus were 25.271.5 mm and 11.970.7 mm, respectively. All the netted dog whelks were, presumably, at least 4 years old and sexually mature, on the basis of the study of Tallmark (1980). The soft tissues of molluscs were excised with stainless-steel scalpel blades, thoroughly rinsed with MilliQ water to remove extraneous impurities and homogenized using a blender (Ultraturrax). The homogenized samples were kept at –20 1C until analysis. 2.3. Analytical procedures Grain-size analyses were performed in each original sediment sampled through a laser diffraction sizer (Malvern Mastersizer 2000 coupled with Hydro 2000 s sampler unit) after 48 h of hydrogen peroxide treatment to reduce organic matter, and removal of organic debris and shell fragments by sieving ( o2 mm). Total carbon (Ctot), and total nitrogen (Ntot) were determined by a CHNSO elemental analyzer (Fisons mod. EA1108, Italy). Organic carbon (Corg) was determined as total carbon after removal of carbonates with HCl, according to the procedure described by Nieuwenhuize et al. (1994). Acetanilide was used as a standard for carbon and nitrogen determinations. The reproducibility was o2%. Reference material BCSS (CNRC, Canada) was used to assess the accuracy of carbon and nitrogen analysis (respectively, 95% and 90%). The indicative values reported by Nieuwenhuize et al. (1994) were used as reference. Corg and Ntot concentrations in sediments were expressed as weight percentage of the element on the dry sediment. About 50 mg of the dry sediment was submitted to acid digestion using a mixture of concentrated HCl (34%, Carlo Erba, Superpure), HNO3 (70%, Carlo Erba, Superpure) and HF (48%, BDH Aristar) (2:0.5:0.1 v/v). Boric acid (0.6% w/v, BDH Suprapur) was added in a second stage only in the sediment digestion (adapted from Mester et al. (1999)). Concentrated HNO3 (70%, Carlo Erba, Superpure) for the dried biota soft tissue (500 mg) was used (Navarro et al., 1992). The digestion was performed by teflon bombs with a microwave oven Milestone 1200 in pressure-controlled conditions. Digested samples were diluted to 50 mL with MilliQ water and analyzed for metal contents. Analysis of chromium (Cr), zinc (Zn), copper (Cu), iron (Fe), was determined by atomic emission spectroscopy of inductively coupled plasma (ICP-AES) while lead (Pb) was determined by graphite furnace atomic absorption spectrometry (GFAAS). Procedural blanks were run within each batch. The analytical precision was estimated by repeated analyses of both samples and standard solutions. Analytical precision gave a mean error of 5% for

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D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

SOUTHERN VENICE LAGOON

ADRIATIC SEA

Tidal inlet

CHIOGGIA TOWN

Brenta River mouth

Adige River mouth

Fig. 1. Sampling stations in the southern Venice lagoon.

Table 1 Accuracy (%) of analytical method for different metals in certified reference materials, marine sediment (BCSS, PACS-2 and, MESS-2, NRC, Canada) and oyster tissue (1566a, NBS, USA) determined by graphite furnace atomic absorption spectrometry and inductively coupled plasma-atomic emission spectrometry. Metal

BCSS 1

PACS-2

MESS-2

Oyster tissue

Pb Cra Cua Zna Fea

 79 72 89 94

95 106 91 92 95

 107 91 87 90

97 105 90 97 100

a

Determined by inductively coupled plasma-atomic emission spectrometry.

all metals. Certified reference materials, marine sediment (BCSS, PACS-2 and MESS-2, NRC, Canada) and oyster tissue (1566a, NBS, USA), were used to control the accuracy of the analytical method (Table 1). Concentrations of metals were expressed as mg kg  1 of dry sediments and biota.

2.4. Sediment enrichment factor In order to estimate the contamination degree due to anthropogenic inputs in sediments, the non dimensional enrichment factor (EF) was determined for each metal by the following ratio: ðMe=NÞsample =ðMe=NÞbaseline where Me is the concentration of the potentially enriched metal and N is the concentration of the normalizing element. A value of 1 denotes no enrichment or depletion relative to the local background level (baseline). Iron (Fe) was chosen as the normalizing element due to its significant correlation with the o16 mm fraction (r2 ¼0.87; p o0.001), which is the finest grain-size component. Normalization of metal concentrations accounts for grain-size variability prior to assessing the degree of contamination. The metal baseline value for the lagoon sediments were estimated from metal concentrations in the deepest strata of the radiodated cores (pre-industrial values, Donazzolo et al., 1982) and from reference values reported in the literature for non polluted sediments (Pavoni et al., 1992 and references therein).

D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

2.5. Biota-Sediment-Accumulation-Factor The Biota-Sediment-Accumulation-Factor (BSAF) is an adimensional ratio between metal concentrations in tissues and in sediments (Thomann et al., 1995). BSAF is a parameter describing bioaccumulation of sediment-associated organic compounds or metals into tissues of ecological receptors and the BSAF definition does not involve or include the assumption of equilibrium conditions for the chemical between the organism and the sediment (Thomann et al., 1992). The BSAF according to Thomann et al. (1995) was calculated as follows:

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and gastropods, as number of cases was different between samples and data distribution was not normal (Shapiro–Wilk test, p o0.05). Correlation analyses (Spearman correlation coefficient) were tested to characterize sediments (mud (o62.5 mm) content vs. Corg and Ntot), for metals vs. muddy fraction and Corg, and for metal concentrations in sediments vs. gastropods.

3. Results and discussion

BSAF ¼ ðMegastropod Þ=ðMeediment Þ

3.1. Sediments characteristics

where Me is the concentration (mg kg  1) of the metal Me expressed on the dry weight basis. In the present study, we also calculated a normalized accumulation factor (BSFAn) in order to take into account the chemical and physical variability in the composition of the sedimentary environment. The BSAFn has been calculated as follows:

According to Shepard’s sediment classification (1954), sandy silt and silt textural types were prevalent inside the lagoon, while sands and silty sands were the predominant textures in sea coastal area samples. A clay component was present in reduced amount (o7%) in all sediment samples. Grain-size progressively decreased from the tidal inlet towards the inner areas of the lagoon. Very fine to medium sands were only found in the marine area and in some sites near Chioggia town. Most of the samples were characterized by a high percentage of very fine silt (2–8 mm) particles. The Corg/Ntot molar ratios calculated on the basis of the Corg (0.3–3.1%) and Ntot (0.02–0.38%) contents ranged from 5.3 to 13.7. In lagoon sediments, the C/N ratio was lower than 10, which suggests a higher contribution from the marine organic component, mainly derived from the decomposition of macroalgae (Sfriso et al., 1994). Sand-silt sediments in dockyards were the most enriched in Corg, whereas the sandy sediments of harbours showed the lowest values of Corg

BSAF n ¼ ðMegastropod Þ=ðMesediment =mudÞ where the metal concentration in sediment was a normalized element for the mud content ( o62.5 mm expressed as g g  1). 2.6. Statistical analyses STATISTICA software (ver 6.0, StatSoft Inc., Tulsa, OK, USA) was used for statistical processing. Non-parametric Mann–Whitney U tests were used to compare metal concentrations in sediments

Table 2 Main sediment characteristics related to grain-size and organic matter. Mean concentrations and standard deviations are reported for each parameter. Parameter

Dockyards–Harbours (n ¼6)

Marina (n ¼4)

Urban area (n ¼6)

Lagoon channels (n¼ 11)

Coastal area (n¼ 7)

Sand (%) Silt (%) Clay (%) Corg (%) Ntot (%) Corg/Ntot (mol/mol)

34.2 7 29.6 61.3 7 27.9 4.6 7 1.8 1.6 7 1.2 0.17 7 0.12 9.6 7 3.1

40.17 35.3 55.77 32.7 4.17 2.7 1.27 1.1 0.167 0.11 9.07 2.9

38.9 7 37.0 56.6 7 34.2 4.67 2.9 1.67 1.1 0.207 0.14 9.97 2.1

31.97 15.1 63.27 14.2 4.97 1.1 1.67 0.8 0.257 0.08 7.47 1.7

95.47 5.8 4.37 5.2 0.27 0.6 0.17 0.1 0.027 0.01 7.47 1.7

400 350

1537 outlier

300

mg kg−1

250 200 150 100 50 0

DockyardsHarbours

Marina

Urban area

Lagoon channels

Sea coastal area

Zn

184

164

110

104

40

Cu

291

105

44

19

4

Cr

99

83

85

77

37

Pb

100

63

23

53

13

Fig. 2. Metals concentrations (mg kg  1 d.w.) in the sediments of the southern Venice lagoon. Mean values and standard deviations are represented.

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D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

Zn (mg kg-1 )

600

Dockyards Harbours

500

Marina

400 Dockyards Harbours r = 0.886; p <0.05 Lagoon channels r = 0.847; p <0.05 Dockyards Harbours, Urban area, Lagoon channels, Sea-coastal area r = 0.834; p <0.05 y = -28.701+119.181*log10(x)

300 200 100

Centre town Lagoon channels Sea-coastal area

0 0

200

400

600

800

Zn (mg kg-1 )

Cu (mg

1000

1200

1400

1600

kg-1 )

600 500

Dockyards Harbours Marina

400

Centre town

300 200

Dockyards Harbours r = 0.904; p <0.05 Dockyards Harbours, Urban area, Lagoon channels, Sea-coastal area r = 0.835; p <0.05

100 0 0

100

200

300

Lagoon channels Sea-coastal area

400

500

Cr (mg kg-1 )

Pb (mg kg-1 )

160 140 120 100 80 60 40 20 0

Dockyards Harbours Marina Centre town Lagoon channels

Dockyards Harbours, Urban area, Lagoon channels, Sea-coastal area r = 0.669; p <0.05

0

100

200

300 Pb (mg

400

Sea-coastal area

500

kg-1 )

Fig. 3. Relationships among metals in the sediments of Dockyards–Harbours, Marina, Urban area, Lagoon channels and Sea coastal area in the southern Venice lagoon.

12 EF 10

8

6

4

2

0 Cr Dockyards-Harbours

Pb Marina

Urban area

Zn

Cu

Lagoon channels

Sea-coastal area

Fig. 4. Enrichment factor (EF) for copper (Cu), zinc (Zn), chromium (Cr) and lead (Pb) in sediments at Dockyards–Harbours, Marina, Urban area, Lagoon channels and Sea coastal areas.

(Table 2). It cannot be excluded that the highest Corg/Ntot values found in dockyards and urban area sediments were caused by a local source of organic matter such as the debris generated in the use of antifouling paints (Yebra et al., 2004). Solvents included turpentine oil, naphtha, and benzene, linseed oil, shellac varnish, tar, and

various kinds of resin were used as binders (Woods, 1952) in the antifouling paints based on the idea of dispersing a toxicant in a polymeric vehicle. Positive correlation was found between mud (o62.5 mm) content, Corg (r2 ¼0.792; po0.05) and Ntot (r2 ¼0.854; po0.05), suggesting a prevailing association of organic matter with

D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

the finer fraction of the sediments, as reported for other coastal zone of the Northern Adriatic (e.g. Faganeli et al., 1991; Giani et al., 2009). 3.2. Metals in surface sediments Dockyards and Marina sites showed the highest concentrations of Cu, Zn and Pb in the sediments (Fig. 2), as already reported also for Hg (Berto et al., 2007), suggesting a possible past or recent use of these metals by anthropogenic activities. In fact, when it was realized that TBT was having deleterious effects, Cu and other metals, such as Zn, in combination with various organic boosting co-biocides for fouling control (Evans et al., 2000; Yebra et al., 2004) were introduced as the main components of anti-fouling paints. As Cu-based paint has increased in use, its effects on the environment have begun to be examined. In Singapore, high concentrations of Cu and Zn in sediments were related to the high boat traffic and to the use of these elements in anti-fouling paints (Goh and Chou, 1997). In the last years, the release of metals from the industrial plants has been reduced and the polluted sediments stored in the industrial channels are presently the most likely source of toxic metals for the lagoon environment (Bellucci et al., 2002). Although high Pb concentrations were determined in the Dockyards–Harbours and Marina stations with respect to the Lagoon channels and Sea costal area, these values are lower than those reported by Bellucci et al. (2002) for the channels near the industrial area of Porto Marghera, along the inner shoreline of the Venice lagoon where many chemical and petrochemical companies are located. The pattern of Pb fluxes showed clear declines in Italy, as the use of unleaded gasoline has begun in 1990. Cochran et al. (1998) reported that the atmospheric supply can completely account for Cu and Pb deposition in the marsh and lesser amounts of Zn. These patterns reflect both regional trends in the atmospheric transport of trace metals and, perhaps, local atmospheric inputs from the industrial development of Porto Marghera, near Venice. Cu, Zn, Cr and Pb appeared significantly correlated (0.662o r2 o0.888; po0.05) with the muddy fraction and the Corg content in the Lagoon channels and in the Sea coastal sediments, whereas the same parameters were not highly correlated in Dockyards, Marina and Urban sites, probably due to the anthropogenic resuspension of sediments. The relationships between couples of metal concentrations, considering separately those areas mostly impacted by human activities linked with antifouling paints (Dockyards, Marina and Urban areas) and areas more distant from the potential contamination sources (Lagoon Channels and Sea coastal area), showed significant correlations (po0.05) for almost all the metals, particularly for Cu and Zn (Fig. 3) in the Dockyards–Harbours sites. No significant relationship has been found for Cr and Cu even if antifouling paint and pressure treated wood could contain Cr. Among the metals analyzed, the highest values of EFs ( 410) were found for Cu near the Dockyards–Harbours and Marina sites, whereas the lowest enrichments were observed in the Sea coastal area (Fig. 4). Dispersal of sediments due to anthropogenic activities resulting from the combination of dredging and mechanical clam harvesting in the central sector of the Venice Lagoon, (Bloom et al., 2004; Sfriso et al., 2005) may have contributed to increase the metal EF values in the channels of the southern lagoon, as already reported for Hg by Berto et al. (2006). Similarly, Pb, Cr and Zn showed high EF values, although lower than Cu, with a decreasing trend proceeding towards less impacted sites, thus suggesting an apparent gradient of the anthropogenic inputs and, especially for Cu, which support the hypothesis of a recent major use of antifouling tin free compounds (Fig. 4) in the Dockyards– Harbours and Marina sites. Conversely, EF values of Cr constantly higher than 1 in all sites with respect to the background value, suggest a diffuse anthropogenic contribution of this metal which

39

seems not referable to the local sources. A side-effect due to mechanical clam harvesting, as reported by Bernardello et al. (2006), could have contributed to increase Cr abundance in sediments of the investigated area. This evidence is also supported by the strong correlation observed between Cr and Ni (r2 ¼0.825, p o0.001, Berto, unpublished data). Besides, discharge of Cr by tanneries in the Brenta and Adige rivers, whose mouths are located south of the Chioggia inlet (Donazzolo et al., 1982), cannot be excluded as further metal contribution thus explaining the higher EF for Cr found in sediments, particularly in the investigated sea coastal area (Fig. 1).

3.3. Metals in gastropods In agreement with the results obtained from sediments, gastropod samples showed higher levels of Cu and Zn in the impacted sites (8007318 mg kg  1 and 5767129 mg kg  1) with respect to those collected in lagoon channels (341716 mg kg  1; 51378 mg kg  1) and sea coastal area (164748 mg kg  1;

a 1000.0 Dockyards-Harbours-Marina-Urban area Lagoon Channels

BSFAn

Sea-coastal area

100.0

10.0

1.0

0.1

0.0 Cu

Zn

Cr

Pb

b 100.0 Dockyards-Harbours-Marina-Urban area Lagoon Channels

BSFA

Sea-coastal area

10.0

1.0

0.1

0.0 Cu

Zn

Cr

Pb

Fig. 5. Mean values of the Biota-Sediment-Accumulation-Factor (BSFA) for metals in sediments and in netted dog whelks of the southern Venice lagoon. (a) BSFAn, metals’ concentrations in sediments normalized for mud ( o62.5 mm) content and (b) BSAF not normalized.

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D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

Fig. 6. Relationship between Cu concentrations in the sediments and in the netted dog whelks.

4747188 mg kg  1). Cr and Pb did not show a significant difference (test U Mann Whitney p 40.05) of concentrations between impacted (1374 mg kg  1; 1.5 70.4 mg kg  1, respectively) and less impacted sites (773 mg kg  1; 1.270.8 mg kg  1). Cu and Zn concentrations, found in gastropods collected in the area of our study were 176 and 5 folds higher, respectively, than the concentrations found in Mytilus galloprovincialis from the southern Venice lagoon, as reported by Widdows et al. (1997), suggesting that these metals may be biomagnified during their trophic transfer from bivalves to gastropods. Mean Biota-Sediment-Accumulation-Factor (BSAF) values were grouped according to the typology of the anthropogenic impact at the sampling sites (human activities linked to antifouling paints vs diffuse contamination). When plotting BSAF (Fig. 5a) and BSAFn (Fig. 5b), normalized for the content of the muddy fraction, sampling sites are better discriminated. The highest BASFn values were found for Cu and Zn in Dockyards–Marina and Lagoon channel whereas the lowest ratios were achieved in the coastal area, where sediments were mainly sandy. These results pointed out that chemical and physical features of bottom sediments could play an important role in the potential transfer of metals from sediments to gastropods. Cu and Zn showed higher BSAF than the other metals, as also reported by Thomann et al. (1995) in bivalves, although a positive correlation between metal concentrations in sediments and in gastropods was found only for Cu (Fig. 6). The dog whelk lives on the sediment and frequently burrows in it, which favours the accumulation of metals from this source. However, it is well known that N. reticulatus changes food preferences in relation to its size: even if small snails are particularly attracted by detritus with a relative high content of organic matter, larger netted dog whelks (more than 25 mm of length), as those collected in this study, shift they preferences to carrion (Tallmark, 1980). These results could be due to a high assimilation efficiency of Cu and Zn from food, relatively low depuration rate, as also found for Zn and Cd in other marine predatory gastropods by Wang and Ke (2002). Though the mechanisms for the metal assimilation efficiency in the gastropods are not exactly understood, several studies have demonstrated that the cytosolic metallothioinein like proteins and the presence of a non-metallothionein-like metal binding protein in the gastropod N. reticulatus also

contribute considerably to the high assimilation efficiency of metals in the gastropods that contain an exceedingly high concentration of metals such as Cu and Zn (Wang and Ke, 2002; Wang and Rainbow, 2000). Moreover, the relatively great toxicity of Cu to N. reticulatus could possibly be explained by a greater accumulation rate of Cu, with the gills as the main target organ (Cheung et al., 2002). In contrast, N. reticulatus is more tolerant to the exposure of Zn, because it can regulate exposure of the gills by redistributing the excess Zn to different parts of the body such as the hepatopancreas, intestine, gills and foot (Kaland et al., 1992). Since the regulatory ability of gastropods for essential metals should be taken into account especially when using gastropods as indicator for Zn and Cu (Wilson, 1982; Soto et al., 1997).

4. Conclusions High concentrations of Cu, Zn, and Pb along with high corresponding enrichment factors (EFs) determined at the surface sediments of Dockyards–Harbours and Marina sites may indicate a local source of contamination of these metals that could be attributed to their recent use in the antifouling tin free paints or coating paints. However, also resuspension due to dredging of channels and Manila clam harvesting by mechanical gears in the central lagoon could facilitate the transport and spreading of contaminants in the southern Venice lagoon. This is evident for Cr, whose enrichment values higher than 1 are widely distributed in the investigated area. N. reticulatus, a scavenger benthic gastropod, showed high concentrations of metals, in particular of Cu, as observed in sediments. A significant correlation and relevant biota-sediment accumulation factor from the sediments to the snails was observed for Cu. Taking into account the size and food preferences of whelks, the elevated concentrations of metals, especially for Cu, could also indicate a prevalent accumulation along the first step of the benthic trophic chain. Considering the widespread presence of N. reticulatus throughout the lagoon, the results from this study show that this species could provide valuable information about the bioavailability of metals and their accumulation through the benthic trophic chain. In order to improve the management of contaminated sediments, there would be a need of further research to better

D. Berto et al. / Continental Shelf Research 45 (2012) 34–41

discriminate the source of metals contamination identifying the contribution derived from the central lagoon and from the atmospheric deposition vs past e new activities of the southern Venice lagoon such as dockyards, harbours and marinas sites. Moreover, after the TBT experience, policies monitoring studies should be developed in order to regulate biocides avoiding damage to the marine environment.

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