Tin free antifouling paints as potential contamination source of metals in sediments and gastropods...

Continental Shelf Research ] (]]]]) ]]]–]]]

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Research papers

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

Daniela Berto a,n, Rossella Boscolo Brus�a 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, Italyb Dipartimento di Matematica e Geoscienze, Via Weiss 2, 34128 Trieste, Italyc Istituto Nazionale di Oceanografia e Geofisica Sperimentale, 34151 Trieste, Italy

a r t i c l e i n f o

Article history:

Received 1 September 2011

Received in revised form

21 May 2012

Accepted 28 May 2012

Keywords:

Antifouling paints

Gastropods

Nassarius reticulatus

Accumulation factor

Venice lagoon

Metals

43/$ - see front matter & 2012 Elsevier Ltd. A

x.doi.org/10.1016/j.csr.2012.05.017

esponding author.

ail address: [email protected] (D.

e cite this article as: Berto, D., et alopods of the southern Venice lagoo

a b s t r a c t

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 (EF410) 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-Accumulation-

Factor 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.

1. Introduction

Anthropogenic heavy metals have been introduced into theaquatic environment directly by industrial activities, sewagetreatments, urban discharges, atmospheric depositions and alsoby 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 inantifouling paints (Yebra et al., 2004). However, such compoundspose severe environmental and human health risk, and they werevoluntarily withdrawn by the paint industry during the early1960s (Bennett, 1996). They were largely replaced by tributyltin(TBT) compounds (Hoch, 2001). Considering the high toxicity ofTBT-based antifouling paints, their use was banned since 2003and phased out on all vessels since 2008 (Reg. EC 782/2003). Theconcern over the harmful side effects of TBT on the aquaticenvironment has resulted in significant development of TBT-freesystems (Evans et al., 2000; Yebra et al., 2004) resulting in the re-use of other metal based antifouling paints, like copper (Cu)-based paints (Yebra et al., 2004 and authors therein). Copperoxide is the most used biocide in the composition of these

ll rights reserved.

Berto).

., Tin free antifouling paintn. Continental Shelf Researc

paints (Boxall et al., 2000; Schiff et al., 2004) but zinc (Zn)-basedantifouling compounds are also used (Yebra et al., 2004 andtherein authors).

A list of the most commonly used nontoxic pigments in shipbottom paints as zinc oxide, zinc dust, iron oxides, silica, andmagnesium silicate were reported by ADAMSON (1922, 1937).Moreover the Zn compounds are more frequently a part of theanticorrosive, but may also be used in the antifouling coatings.With regard to the soluble pigment Zn(II) oxide, there is a totallack of studies on its behaviour in sea water (e.g. dissolution rate)and its consequent effect on antifouling paint whereas its use assacrificial anode on boat motors is well known.

In addition to these, pigments such as chrome green, chromeyellow, and various lakes may be used for inert and colouringpurposes in association with organotins polymers and antifoulingpaints Turner et al., 2009).

Lead finds its way into the aquatic environment via atmo-spheric inputs as well as from leaded gas leaking from boats (Pbwas not phased out of use in boats until the late 1980s).

Several works described the sediment contamination bymetals in the northern and central Venice lagoon (e.g. Bellucciet al., 2002; Pavoni et al., 1992) but a few studies addressed to thesouthern area (Berto et al., 2006, 2007). The intense ship traffic(1.106 t y�1) due to the presence of the Chioggia harbour, smallferries and the presence of many marinas, dockyards and

s as potential contamination source of metals in sediments andh (2012), http://dx.doi.org/10.1016/j.csr.2012.05.017

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shipyards added with the most important fishing fleet (APAT,2005) of northern Adriatic sea contribute to increase the potentialrisk of contamination in the surface sediments of this area in thelast decades. Harvesting of Manila clam (Tapes philippinarum) bymean of specific gears is an important cause of resuspension ofbottom sediments (Pranovi et al., 2004) causing erosion in thecentral lagoon with a global sediment loss of ca. 1.2 million -tonnes year�1 (Sfriso et al., 2005). More recently, in order tocreate a new commercial harbour in the Chioggia area, intensedredging has become a very common activity causing relevantsediment resuspension which can be responsible for metalsrelease from sediments into the water column. However, theknowledge of the distribution of heavy metals in sediments doesnot allow determining the real extent of their bioavailability and,consequently, the toxicity and risk of their accumulation into theaquatic trophic chain (Blackmore, 1998).

Different organisms and species show different responsemechanisms to metal ions and organisms which accumulatemetals in their tissues and may therefore be analyzed as ameasure of bioavailability of metals in the habitat (Rainbow,1995). Circumstantial evidences indicated that concentrations ofseveral metals (e.g. Cd, As, Cr, and Zn) in marine gastropods canbe higher than concentrations measured in marine bivalves thatare 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 ofbottom sediments at water depths of 0–20 m (de Kluijver et al.,2000), could be used for biomonitoring coastal contamination dueto its capacity in accumulating heavy metals (Kaland et al., 1992).The distribution area of this snail extends in the Atlantic Oceanfrom Norway to Morocco. This species lives in the North Sea, theKattegat and western Baltic Sea, Black Sea and Mediterranean Sea(e.g., de Kluijver et al., 2000) and it has been used in TBTmonitoring 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, especiallymercury (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 anthro-pogenic inputs, in the surface sediments of the southern VeniceLagoon and their bioaccumulation in gastropods N. reticulatus, inorder to understand whether the relevant use of marine antifoul-ing tin-free biocide-based products has contributed to increasemetals abundance contents in this lagoon environment.

2. Materials and methods

2.1. Study area

The Venice lagoon (Northern Adriatic Sea, Italy) is a transi-tional coastal environment covering a surface area of 549 km2 andit is characterized by a network of channels of various depths,estuaries, salt marshes and mudflats; the mean water depth isabout 0.6 m, and the tidal range is less than 1 m. Three inletsconnect the lagoon with the open sea (Lido, Malamocco andChioggia, from north to south with mean depth 14, 17 and 8 mrespectively). Major man-made transformations have especiallytaken place since the 1940: large chemical and metallurgicindustrial plants were established at the edge of the lagoon (thePorto Marghera industrial district); a deep canal (Canale deiPetroli) was dug across the lagoon to serve the industrial district.

The study area is located in the southern basin of the Venicelagoon, near the town of Chioggia (53,470 inhabitants, Fig. 1),affected by a constant increase in dockyards, harbours, marinasand shipping activities in the recent years. Moreover, the central

Please cite this article as: Berto, D., et al., Tin free antifouling paintgastropods of the southern Venice lagoon. Continental Shelf Researc

and southern lagoons have been deeply affected by Manila clamsharvesting since the end of the 1980, based on mechanicaltechniques that cause resuspension and mixing of surface sedi-ments down to several centimetres depth. This activity along withdredging operations recently performed in the southern basin ofthe Venice lagoon may have largely made possible diffusion ofcontaminants.

2.2. Sampling

Samples were collected in the southern Venice lagoon and incoastal area of Adriatic Sea from April to September 2003.Sampling sites were distinguished as Dockyards, Harbours, Mar-ina, Urban area, Lagoon channels and Sea-coastal area on the basisof their location and human activities involved (Fig. 1).

Sediments were sampled by an Ekman grab at 34 sites. The upper2–3 cm were recovered and collected into acid-cleaned glass contain-ers, rapidly homogenized, sieved through 200 mm nylon net and keptat –20 1C until analysis. Pools of 20–40 specimens of netted dogwhelk, N. reticulatus were caught by a wire basket at 11 of the 36 siteswhere sediments were sampled. The mean shell length and width ofall the collected specimens of N. reticulatus were 25.271.5 mm and11.970.7 mm, respectively. All the netted dog whelks were, pre-sumably, at least 4 years old and sexually mature, on the basis of thestudy of Tallmark (1980). The soft tissues of molluscs were excisedwith stainless-steel scalpel blades, thoroughly rinsed with MilliQwater to remove extraneous impurities and homogenized using ablender (Ultraturrax). The homogenized samples were kept at –20 1Cuntil analysis.

2.3. Analytical procedures

Grain-size analyses were performed in each original sedimentsampled through a laser diffraction sizer (Malvern Mastersizer2000 coupled with Hydro 2000 s sampler unit) after 48 h ofhydrogen peroxide treatment to reduce organic matter, andremoval of organic debris and shell fragments by sieving(o2 mm). Total carbon (Ctot), and total nitrogen (Ntot) weredetermined by a CHNSO elemental analyzer (Fisons mod.EA1108, Italy). Organic carbon (Corg) was determined as totalcarbon after removal of carbonates with HCl, according to theprocedure described by Nieuwenhuize et al. (1994). Acetanilidewas 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 nitrogenanalysis (respectively, 95% and 90%). The indicative valuesreported by Nieuwenhuize et al. (1994) were used as reference.

Corg and Ntot concentrations in sediments were expressed asweight percentage of the element on the dry sediment.

About 50 mg of the dry sediment was submitted to acid diges-tion using a mixture of concentrated HCl (34%, Carlo Erba, Super-pure), 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 asecond stage only in the sediment digestion (adapted from Mesteret al. (1999)). Concentrated HNO3 (70%, Carlo Erba, Superpure) forthe dried biota soft tissue (500 mg) was used (Navarro et al., 1992).The digestion was performed by teflon bombs with a microwaveoven Milestone 1200 in pressure-controlled conditions. Digestedsamples were diluted to 50 mL with MilliQ water and analyzed formetal contents. Analysis of chromium (Cr), zinc (Zn), copper (Cu),iron (Fe), was determined by atomic emission spectroscopy ofinductively coupled plasma (ICP-AES) while lead (Pb) was deter-mined by graphite furnace atomic absorption spectrometry (GFAAS).Procedural blanks were run within each batch. The analyticalprecision was estimated by repeated analyses of both samples andstandard solutions. Analytical precision gave a mean error of 5% for


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Table 1Accuracy (%) 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 � 95 � 97

Cra 79 106 107 105

Cua 72 91 91 90

Zna 89 92 87 97

Fea 94 95 90 100

a Determined by inductively coupled plasma-atomic emission spectrometry.

SOUTHERN VENICE LAGOON

Tidal inlet

ADRIATIC SEA

CHIOGGIA TOWN

Adige River mouth

Brenta River mouth

Tidal inlet

Adige River mouth

Brenta River mouth

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

D. Berto et al. / Continental Shelf Research ] (]]]]) ]]]–]]] 3

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 ofdry sediments and biota.


2.4. Sediment enrichment factor

In order to estimate the contamination degree due to anthro-pogenic inputs in sediments, the non dimensional enrichmentfactor (EF) was determined for each metal by the following ratio:

ðMe=NÞsample=ðMe=NÞbaseline

where Me is the concentration of the potentially enriched metaland N is the concentration of the normalizing element. A value of1 denotes no enrichment or depletion relative to the local back-ground level (baseline). Iron (Fe) was chosen as the normalizingelement due to its significant correlation with the o16 mmfraction (r2

¼0.87; po0.001), which is the finest grain-sizecomponent. Normalization of metal concentrations accounts forgrain-size variability prior to assessing the degree of contamina-tion. The metal baseline value for the lagoon sediments wereestimated from metal concentrations in the deepest strata of theradiodated cores (pre-industrial values, Donazzolo et al., 1982)and from reference values reported in the literature for nonpolluted sediments (Pavoni et al., 1992 and references therein).


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2.5. Biota-Sediment-Accumulation-Factor

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

BSAF ¼ ðMegastropodÞ=ðMeedimentÞ

where Me is the concentration (mg kg�1) of the metal Me expressedon the dry weight basis.

In the present study, we also calculated a normalized accumulationfactor (BSFAn) in order to take into account the chemical and physicalvariability in the composition of the sedimentary environment.

The BSAFn has been calculated as follows:

BSAFn ¼ ðMegastropodÞ=ðMesediment=mudÞ

where the metal concentration in sediment was a normalizedelement 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) wasused for statistical processing. Non-parametric Mann–Whitney Utests were used to compare metal concentrations in sediments

Table 2Main sediment characteristics related to grain-size and organic matter. Mean concentr

Parameter Dockyards–Harbours (n¼6) Marina (n¼4)

Sand (%) 34.2729.6 40.1735.3

Silt (%) 61.3727.9 55.7732.7

Clay (%) 4.671.8 4.172.7

Corg (%) 1.671.2 1.271.1

Ntot (%) 0.1770.12 0.1670.11

Corg/Ntot (mol/mol) 9.673.1 9.072.9

Dockyards-Harbours Marina Ur

Zn 184 164Cu 291 105Cr 99 83Pb 100 63

0

50

100

150

200

250

300

350

400

mg

kg−1

1537 outlier

Fig. 2. Metals concentrations (mg kg�1 d.w.) in the sediments of the souther


and gastropods, as number of cases was different betweensamples and data distribution was not normal (Shapiro–Wilktest, po0.05). Correlation analyses (Spearman correlation coeffi-cient) 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

3.1. Sediments characteristics

According to Shepard’s sediment classification (1954), sandy siltand silt textural types were prevalent inside the lagoon, while sandsand silty sands were the predominant textures in sea coastal areasamples. A clay component was present in reduced amount (o7%)in all sediment samples. Grain-size progressively decreased from thetidal inlet towards the inner areas of the lagoon. Very fine tomedium sands were only found in the marine area and in somesites near Chioggia town. Most of the samples were characterized bya 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 contribu-tion from the marine organic component, mainly derived from thedecomposition of macroalgae (Sfriso et al., 1994). Sand-silt sedi-ments in dockyards were the most enriched in Corg, whereas thesandy sediments of harbours showed the lowest values of Corg

ations and standard deviations are reported for each parameter.

Urban area (n¼6) Lagoon channels (n¼11) Coastal area (n¼7)

38.9737.0 31.9715.1 95.475.8

56.6734.2 63.2714.2 4.375.2

4.672.9 4.971.1 0.270.6

1.671.1 1.670.8 0.170.1

0.2070.14 0.2570.08 0.0270.01

9.972.1 7.471.7 7.471.7

ban area Lagoonchannels Sea coastal area

110 104 4044 19 485 77 3723 53 13

n Venice lagoon. Mean values and standard deviations are represented.


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Cu (mg kg-1 )

Zn (m

g kg

-1 )

Dockyards Harbours

Marina

Centre town

Lagoon channels

Sea-coastal area

0 200 400 600 800 1000 1200 1400 16000

100200300400500600

Pb (mg kg-1 )

Zn (m

g kg

-1 )

Dockyards Harbours

Marina

Centre town

Lagoon channels

Sea-coastal area

0 100 200 300 400 5000

100200300400500600

Pb (mg kg-1 )

Cr (

mg

kg-1

)

Dockyards Harbours

Marina

Centre town

Lagoon channels

Sea-coastal area

0 100 200 300 400 5000

20406080

100120140160

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

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

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

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.

0

2

4

6

8

10

12

Cr Pb Zn Cu

EF

Dockyards-Harbours Marina Urban area 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 valuesfound in dockyards and urban area sediments were caused by a localsource of organic matter such as the debris generated in the use ofantifouling paints (Yebra et al., 2004). Solvents included turpentineoil, naphtha, and benzene, linseed oil, shellac varnish, tar, and


various kinds of resin were used as binders (Woods, 1952) in theantifouling paints based on the idea of dispersing a toxicant in apolymeric vehicle. Positive correlation was found between mud(o62.5 mm) content, Corg (r2

¼0.792; po0.05) and Ntot (r2¼0.854;

po0.05), suggesting a prevailing association of organic matter with


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0.0

0.1

1.0

10.0

100.0

1000.0

BSFAn Dockyards-Harbours-Marina-Urban areaLagoon Channels Sea-coastal area

0.0

0.1

1.0

10.0

100.0

Cu

BSFA Dockyards-Harbours-Marina-Urban areaLagoon Channels Sea-coastal area

a

b

PbCrZn

Cu PbCrZn

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.


the finer fraction of the sediments, as reported for other coastal zoneof 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 concentra-tions of Cu, Zn and Pb in the sediments (Fig. 2), as alreadyreported also for Hg (Berto et al., 2007), suggesting a possiblepast or recent use of these metals by anthropogenic activities. Infact, when it was realized that TBT was having deleterious effects,Cu and other metals, such as Zn, in combination with variousorganic boosting co-biocides for fouling control (Evans et al.,2000; Yebra et al., 2004) were introduced as the main compo-nents of anti-fouling paints. As Cu-based paint has increased inuse, its effects on the environment have begun to be examined. InSingapore, high concentrations of Cu and Zn in sediments wererelated to the high boat traffic and to the use of these elements inanti-fouling paints (Goh and Chou, 1997).

In the last years, the release of metals from the industrialplants has been reduced and the polluted sediments stored in theindustrial channels are presently the most likely source of toxicmetals for the lagoon environment (Bellucci et al., 2002).

Although high Pb concentrations were determined in theDockyards–Harbours and Marina stations with respect to the Lagoonchannels and Sea costal area, these values are lower than thosereported by Bellucci et al. (2002) for the channels near the industrialarea of Porto Marghera, along the inner shoreline of the Venice lagoonwhere many chemical and petrochemical companies are located. Thepattern of Pb fluxes showed clear declines in Italy, as the use ofunleaded gasoline has begun in 1990. Cochran et al. (1998) reportedthat the atmospheric supply can completely account for Cu and Pbdeposition in the marsh and lesser amounts of Zn. These patternsreflect both regional trends in the atmospheric transport of tracemetals and, perhaps, local atmospheric inputs from the industrialdevelopment of Porto Marghera, near Venice.

Cu, Zn, Cr and Pb appeared significantly correlated (0.662or2o0.888; po0.05) with the muddy fraction and the Corg contentin the Lagoon channels and in the Sea coastal sediments, whereas thesame parameters were not highly correlated in Dockyards, Marinaand Urban sites, probably due to the anthropogenic resuspension ofsediments. The relationships between couples of metal concentra-tions, considering separately those areas mostly impacted by humanactivities linked with antifouling paints (Dockyards, Marina andUrban areas) and areas more distant from the potential contami-nation sources (Lagoon Channels and Sea coastal area), showedsignificant correlations (po0.05) for almost all the metals, particu-larly for Cu and Zn (Fig. 3) in the Dockyards–Harbours sites.

No significant relationship has been found for Cr and Cu even ifantifouling paint and pressure treated wood could contain Cr.Among the metals analyzed, the highest values of EFs (410) werefound for Cu near the Dockyards–Harbours and Marina sites,whereas the lowest enrichments were observed in the Sea coastalarea (Fig. 4). Dispersal of sediments due to anthropogenic activ-ities resulting from the combination of dredging and mechanicalclam harvesting in the central sector of the Venice Lagoon, (Bloomet al., 2004; Sfriso et al., 2005) may have contributed to increasethe metal EF values in the channels of the southern lagoon, asalready reported for Hg by Berto et al. (2006). Similarly, Pb, Cr andZn showed high EF values, although lower than Cu, with adecreasing trend proceeding towards less impacted sites, thussuggesting an apparent gradient of the anthropogenic inputs and,especially for Cu, which support the hypothesis of a recent majoruse of antifouling tin free compounds (Fig. 4) in the Dockyards–Harbours and Marina sites. Conversely, EF values of Cr constantlyhigher than 1 in all sites with respect to the background value,suggest a diffuse anthropogenic contribution of this metal which


seems not referable to the local sources. A side-effect due tomechanical clam harvesting, as reported by Bernardello et al.(2006), could have contributed to increase Cr abundance insediments of the investigated area. This evidence is also sup-ported by the strong correlation observed between Cr and Ni(r2¼0.825, po0.001, Berto, unpublished data). Besides, discharge

of Cr by tanneries in the Brenta and Adige rivers, whose mouthsare located south of the Chioggia inlet (Donazzolo et al., 1982),cannot be excluded as further metal contribution thus explainingthe higher EF for Cr found in sediments, particularly in theinvestigated 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 theimpacted sites (8007318 mg kg�1 and 5767129 mg kg�1) withrespect to those collected in lagoon channels (341716 mg kg�1;51378 mg kg�1) and sea coastal area (164748 mg kg�1;


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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 differ-ence (test U Mann Whitney p40.05) of concentrations betweenimpacted (1374 mg kg�1; 1.570.4 mg kg�1, respectively) andless impacted sites (773 mg kg�1; 1.270.8 mg kg�1).

Cu and Zn concentrations, found in gastropods collected in thearea of our study were 176 and 5 folds higher, respectively, thanthe concentrations found in Mytilus galloprovincialis from thesouthern Venice lagoon, as reported by Widdows et al. (1997),suggesting that these metals may be biomagnified during theirtrophic transfer from bivalves to gastropods.

Mean Biota-Sediment-Accumulation-Factor (BSAF) values weregrouped according to the typology of the anthropogenic impact atthe sampling sites (human activities linked to antifouling paintsvs 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 valueswere found for Cu and Zn in Dockyards–Marina and Lagoonchannel whereas the lowest ratios were achieved in the coastalarea, where sediments were mainly sandy. These results pointedout that chemical and physical features of bottom sedimentscould play an important role in the potential transfer of metalsfrom sediments to gastropods.

Cu and Zn showed higher BSAF than the other metals, as alsoreported by Thomann et al. (1995) in bivalves, although a positivecorrelation between metal concentrations in sediments and ingastropods was found only for Cu (Fig. 6). The dog whelk lives onthe sediment and frequently burrows in it, which favours theaccumulation of metals from this source. However, it is wellknown that N. reticulatus changes food preferences in relation toits size: even if small snails are particularly attracted by detrituswith a relative high content of organic matter, larger netted dogwhelks (more than 25 mm of length), as those collected in thisstudy, shift they preferences to carrion (Tallmark, 1980).

These results could be due to a high assimilation efficiency ofCu and Zn from food, relatively low depuration rate, as also foundfor Zn and Cd in other marine predatory gastropods by Wang andKe (2002). Though the mechanisms for the metal assimilationefficiency in the gastropods are not exactly understood, severalstudies have demonstrated that the cytosolic metallothioineinlike proteins and the presence of a non-metallothionein-likemetal binding protein in the gastropod N. reticulatus also


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

4. Conclusions

High concentrations of Cu, Zn, and Pb along with highcorresponding enrichment factors (EFs) determined at the surfacesediments of Dockyards–Harbours and Marina sites may indicatea local source of contamination of these metals that could beattributed to their recent use in the antifouling tin free paints orcoating paints. However, also resuspension due to dredging ofchannels and Manila clam harvesting by mechanical gears in thecentral lagoon could facilitate the transport and spreading ofcontaminants in the southern Venice lagoon. This is evident forCr, whose enrichment values higher than 1 are widely distributedin the investigated area. N. reticulatus, a scavenger benthicgastropod, showed high concentrations of metals, in particularof Cu, as observed in sediments. A significant correlation andrelevant biota-sediment accumulation factor from the sedimentsto the snails was observed for Cu. Taking into account the size andfood preferences of whelks, the elevated concentrations of metals,especially for Cu, could also indicate a prevalent accumulationalong the first step of the benthic trophic chain. Considering thewidespread presence of N. reticulatus throughout the lagoon, theresults from this study show that this species could providevaluable information about the bioavailability of metals and theiraccumulation through the benthic trophic chain.

In order to improve the management of contaminated sedi-ments, there would be a need of further research to better


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discriminate the source of metals contamination identifying thecontribution derived from the central lagoon and from the atmo-spheric deposition vs past e new activities of the southern Venicelagoon such as dockyards, harbours and marinas sites. Moreover,after the TBT experience, policies monitoring studies should bedeveloped in order to regulate biocides avoiding damage to themarine environment.

Acknowledgements

The work was undertaken with the financial support of theC.I.R.S.PE through ‘‘Patti territoriali specializzati nel settoredell’agricoltura e della pesca dell’area centro sud della Provinciadi Venezia’’. We thank Dr. Lucio Grassia for his help in the fieldwork, and Dr. Gianluca Franceschini for his assistance with theGIS map.

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Tin free antifouling paints as potential contamination source of metals in sediments and gastropods...

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