Accepted Manuscript Trace element occurrence in the Pacific oyster Crassostrea gigas from coastal marine ecosystems in Italy E.A.V. Burioli, S. Squadrone, C. Stella, C. Foglini, M.C. Abete, M. Prearo PII:

S0045-6535(17)31325-5

DOI:

10.1016/j.chemosphere.2017.08.102

Reference:

CHEM 19800

To appear in:

ECSN

Received Date: 11 May 2017 Revised Date:

17 July 2017

Accepted Date: 18 August 2017

Please cite this article as: Burioli, E.A.V., Squadrone, S., Stella, C., Foglini, C., Abete, M.C., Prearo, M., Trace element occurrence in the Pacific oyster Crassostrea gigas from coastal marine ecosystems in Italy, Chemosphere (2017), doi: 10.1016/j.chemosphere.2017.08.102. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Trace element occurrence in the Pacific oyster Crassostrea gigas from coastal marine

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ecosystems in Italy

3 E.A.V. Burioli*, S. Squadrone, C. Stella, C. Foglini, M.C. Abete, M. Prearo

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Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Turin, Italy.

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*Corresponding author: [email protected]

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Abstract

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The Pacific oyster is one of the world’s most widespread bivalves and a suitable species for

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biomonitoring trace elements in marine environments thanks to its bioaccumulation ability. As it is

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also an edible mollusc, concentrations of harmful elements in its tissues must be monitored. For

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these purposes, 464 wild individuals were collected from 12 sites along the Italian coasts. The

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concentration of fourteen trace elements (Al, As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, Sn, Tl, and

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Zn) in their tissues was quantified. Among the three heavy metals, cadmium, lead, and mercury,

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none exceeded the maximum limit for in food set by European Union regulations but Cd in one

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sample from the Varano Lagoon resulted extremely close to this value. Contamination by Hg of the

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northern Adriatic and Orbetello Lagoons was also observed. Moreover, there was a positive

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association between the lagoon’s environmental conditions and the bioaccumulation of this element

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in oysters. Despite the ban instituted 15 years ago on the use of Sn in antifouling paints, this

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element is still present in several marine environments, as demonstrated in the oysters sampled from

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harbour areas. Samples collected from harbours also showed very high concentrations of Cu and Zn

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due to the ability of oysters to accumulate these elements, which have replaced Sn in antifouling

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paints. Analysis of the samples from most sites indicated a low risk of human exposure to harmful

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elements through oyster consumption; nonetheless, chemical sanitary controls should focus

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primarily on Cd, Cu, and Zn.

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ACCEPTED MANUSCRIPT 26 Keywords Bioaccumulation; Bivalve Molluscs; Mediterranean Sea; Human Consumption;

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Biomonitoring; Public Health

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1. Introduction

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Increased awareness of the far-reaching impact of pollution on the environment and human health

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has led to the development and implementation of action programs for the protection of marine

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environments in the last decades. An international framework for addressing threats to marine

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ecosystems is provided by the Global Programme of Action for the Protection of the Marine

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Environment from Land-based Activities (GPA), which was launched in 1995 and is coordinated in

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partnership with the United Nations Environment Programme (UNEP).

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Protecting vulnerable marine areas like coastal lagoons and estuaries is essential for preserving their

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unique biodiversity and developing their potential economic value for aquaculture activities such as

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bivalve farming. However, these environments are often contaminated with a variety of chemical

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substances, including toxic metals, amongst which cadmium (Cd), lead (Pb) or mercury (Hg), and

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metalloids like arsenic (As) pose a potential threat to ecological and public health. Naturally present

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in marine environments, these elements originate from both geogenic processes and anthropogenic

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activities such as agriculture, mining, and industry (Bradl, 2002; He et al., 2005). Through

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contaminated river flows, direct waste discharges, antifouling paints on ship hulls, and atmospheric

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deposition, these elements ultimately reach and pollute coastal marine areas.

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Approximately 30 trace elements influence an organism’s biology in varied ways and can be

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classified as essentials and non-essentials (Fraústo da Silva and Williams, 1993; Tamás and

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Martinoia, 2005). Some trace elements, including cobalt (Co), copper (Cu), chromium (Cr), iron

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(Fe), manganese (Mn), molybdenum (Mo), nickel (Ni), selenium (Se), and zinc (Zn), are essential

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for animal and human biologic functioning (Mertz, 1981; WHO/FAO/IAEA, 1996, Nordberg and

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Nordberg, 2016). The essentiality of arsenic at ultra-trace concentrations remains debated (Gropper

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ACCEPTED MANUSCRIPT et al., 2008). The excessive intake of some essential elements like Cu (Tchounwou et al., 2008) or

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Cr (Patlolla et al., 2009) can lead to cell damage, while exposure to other trace elements like Cd,

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Pb, and Hg, which have no biological functions, can induce serious adverse effects on human and

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animal health (Tchounwou et al., 2001; 2004a; 2004b; 2014; Sutton et al., 2002) even at low levels

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of exposure. For these reasons, As, Cd, Hg, and Pb have been included in the World Health

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Organisation (2010) list of the top ten chemicals of major public health concern.

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Regular seafood consumption is widely considered beneficial for health (Daviglus et al., 2002;

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EFSA, 2014); however, shellfish are a source of exposure to inorganic contaminants (particularly

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As, Cd, Cu, Fe, Hg, Pb, Se, and Zn) that, above certain concentrations, may pose a risk for

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consumer health (FAO, 2005). Recognizing this problem, European Regulation EC/1881/2006 and

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amendments set maximum limits for Cd, Pb, and Hg in food for human and animal consumption.

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However, these elements can also affect marine biota. At the concentrations commonly found in

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water bodies, many have toxic effects on ecological receptors and at high concentrations, they can

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reduce or eliminate sensitive species and impact an ecosystem biodiversity (Peterson, 1986). For

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instance, the early embryo-larval stages of marine invertebrates have been shown to be highly

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sensitive to micropollutants and to heavy metals in particular (Martin et al., 1981; Beiras and His,

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1995).

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Aquatic organisms, being exposed to trace elements from the environment, are often used for

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pollution monitoring studies (Chiarelli and Roccheri, 2014). In fact, they are a useful tool for

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assessing water quality and marine ecosystem health in vulnerable areas such as coastal marine

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regions where anthropogenic activities are concentrated (Rainbow, 1995). Biomonitoring has

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proven to be a valid method to assess environmental contamination by toxic elements and to

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determine the concentration of certain toxic metals and other trace elements in marine organisms

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where they continuously accumulate and concentrate in tissues (Shahidul-Islam and Tanaka, 2004)

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in a time-dependant manner (Rainbow, 1995). Furthermore, the levels of nonessential and essential

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ACCEPTED MANUSCRIPT elements in aquatic biota depend on many other factors, including geographic location, species,

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size, feeding patterns, element form and concentration in a given environment, solubility,

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temperature, salinity, oxygen, organic content in water and sediments, and pH (Luoma, 1983;

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Stanković et al., 2012). Shellfish can accumulate inorganic elements at concentrations several

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orders of magnitude higher than the aquatic medium, particularly in mantle, gills and palps (Rodney

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et al., 2007), and from their filtration feeding habits. Furthermore, being benthic animals, they are

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more exposed to solid and dissolved matter stored in contaminated sediments. While all marine

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invertebrates are known to accumulate trace elements in their tissues, their bioconcentration ability

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is species dependent (Mok et al., 2014).

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Biomonitoring investigations in the Mediterranean Sea have primarily focused on Mytilus

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galloprovincialis as a “sentinel” organism (Viarengo et al., 2007). In order to improve our

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understanding of bioaccumulation mechanisms and trace element cycles in the environment, a wider

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range of bioindicators needs to be identified (Conti and Cecchetti, 2003). Numerous studies

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worldwide have successfully used oysters as bioindicator, particularly species of the genus

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Crassostrea such as C. gigas (Beliaeff et al., 1998; Shulkin et al., 2003; Baudrimont et al., 2005),

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C. rhizophorae and C. virginica (Rojas de Astudillo et al., 2005). The Pacific oyster, C. gigas,

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provides an excellent subcosmopolitan “sentinel” species. It is available all year round, abundant in

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numerous marine areas, sessile, can be easily collected, and is extremely resistant to environmental

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stress (Rainbow and Phillips, 1993; Boening, 1999) from high metal exposure as compared to

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mussels (Funes et al., 2006). Nevertheless, the Pacific oyster also raises public health concerns as it

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is one of the most popular bivalve molluscs (http://www.fao.org/figis/servlet/) and diet is one of the

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main routes of exposure to toxic elements for humans. Moreover, few studies to date have been

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performed on C. gigas in the Mediterranean (Ochoa et al., 2013; Squadrone et al., 2016).

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Though the natural beds of C. gigas are quite common along the Italian coast (Burioli et al., 2016),

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commercial Pacific oyster farming is practiced only in three regions, mostly in Sardinia and, to a

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ACCEPTED MANUSCRIPT lesser extent, Veneto and Liguria. Oyster farming has attracted increasing interest due to recent

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awareness of the need for aquaculture diversification. This will require developing new areas, both

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in coastal lagoons and open waters, for oyster farming in the near future. An important part of this

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evaluation process involves the collection of predictive information on trace element

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bioaccumulation that takes onto account both human health and zootechnical aspects.

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With this study, we analysed the trace element occurrence of Al, As, Cd, Cr, Cu, Fe, Mn, Hg, Ni, Pb,

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Se Sn, Tl, and Zn in C. gigas. The sampling areas were 12 sites in five geographical regions with

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different environment features and contamination levels. Considering the growing global concern

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about the effects of pollution on the marine environment, our work contributes to the knowledge of

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trace element occurrence in different marine ecosystems. It provides an assessment of the risk

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associated with oyster consumption and an evaluation of the suitability of the sampling sites as

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potential areas for the further development of mollusc farming activities.

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113 2. Materials and Methods

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2.1. Sampling

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Between May and June 2014, 464 wild individuals of the Pacific oyster, C. gigas, were collected

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along the Italian coasts. The sampling took place during the pre-spawning period. Twelve natural

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oyster beds were sampled and 30 to 60 individuals (≥80 mm in length) were collected from each

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site (Table 1) at a depth of about 0.5 m below the low-water line. A minimum length was

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established in order to collect only those specimens that had resided in the sampling sites for at least

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two years. The specimens were kept alive, immediately placed in a refrigerated box, and processed

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within 24 h. Each individual was externally cleaned with deionized water, shucked, drained, and

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pooled (pools consisted of 5 or 10 whole specimens, based on their singular weight, in order to have

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at least 50 g in each pooled sample) (Table 1), homogenized, and frozen at -20°C until analysis.

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The sampling sites were representative of three different types of marine environment: lagoon, open

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ACCEPTED MANUSCRIPT waters (off-shore and gulfs), and harbour. Eleven sites were located in the Adriatic and one in the

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Tyrrhenian Sea (Figure 1). The sampling sites along the Adriatic coast are described from north to

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south. Muggia and Monfalcone are located in the Gulf of Trieste, a semi-enclosed basin in the

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northern Adriatic. The main freshwater inputs into the Gulf of Trieste are the Isonzo and Timavo

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Rivers. Until 1995, the Isonzo was the primary source of Hg pollution originating from extensive

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mining operations in the upper River drainage basin. The northern and northwest part of the

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Adriatic is characterized by a complex system of transitional environments that includes, amongst

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others, the Marano, Venezia, and Caleri Lagoons. The Marano Lagoon is characterized by shallow

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waters, relatively limited water exchanges with the open sea and several freshwater inputs from the

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Aussa and Corno Rivers, both of which flow through an industrial zone with factories that, for

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many years, manufactured cellulose, chlor-alkali, and artificial textile fibres, the Stella River, and

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various irrigation canals. The Caorle sampling site is located in open waters at about 5 km from the

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coastline. Chemical plants, oil refineries, and shipyards surround the Venice Lagoon, which receives

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freshwater input from the numerous rivers flowing through the highly populated industrial and

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intensive agricultural regions of the Po Plain. Besides altering the salinity and trophic conditions of

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the Lagoon, this input is also an important conduit for the delivery of contaminants to its ecosystem.

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Cavallino-Treporti is located in the less anthropized eastern part of the Lagoon, opposite the city of

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Chioggia. The petrochemical plants clustered within the Marghera industrial zone, where a chlor-

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alkali plant was operated from 1951 to 1988, dominate the central part of the Venice Lagoon. In

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Caleri, as in other parts of the northern lagoons, the water temperature is high and the oxygen

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concentration low in summer, partly due to the shallow water depth but it is mostly influenced by

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open sea environmental conditions because there is no direct entrance of river water at the sampling

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site and good exchanges with the open sea. Porto Garibaldi is near the Po Delta, where sediments

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contain high levels of contaminants from the numerous industrial plants located along the river

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(Guerzoni et al., 1984). Salinity is affected by variations in riverine inputs, with a decreasing impact

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ACCEPTED MANUSCRIPT towards south. Sampling was conducted at the mouth of the canal that connects the Comacchio

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Lagoon with the open sea. In Giulianova the sampling was carried out in the central part of the

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harbour, an enclosed area for both recreational and commercial fishing boats. The Cervia sampling

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site is located in open water, less than 0.5 km from the coast. Finally, Varano Lake communicates

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weakly with the open sea via two artificial canals, one of which is located in Capoiale, where

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sampling was conducted. The area has little industry; the basin receives wastewaters mainly from

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agricultural drainage water. The salinity is less than 30‰ and stable all year round because of the

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presence of underwater springs (Spagnoli et al., 2002). The only sampling site on the Tyrrhenian

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coast is the Orbetello Lagoon. This water body has two communicating basins known as West and

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East, with a1 m average depth, and communicates with the open sea via two canals. The sources of

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anthropogenic contamination are now mainly agriculture wastewaters, but until 1991, a chemical

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factory manufacturing granular fertilizers released waste metals into the western part of the basin. A

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large contribution to the metal contamination of the lagoon also comes from geogenic processes: the

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presence of large cinnabar deposits in the catchment basin of the Albegna River, which flows into

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the lagoon (Grassi and Netti, 2000). Sampling was conducted in the Western lagoon.

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2.2. Detection of trace elements

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Each sample was divided into two aliquots. The first was used for total Hg quantification with a

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direct mercury analyser (DMA-80 Analyser, Milestone, Shelton, CT, USA). The second aliquot was

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used for detecting the other elements (Al, As, Cd, Cr, Cu, Fe, Mn, Ni, Pb, Se, Sn, Tl, and Zn) by

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inductively coupled plasma-mass spectrometry (ICP-MS Xseries II, Thermo Scientific, Bremen,

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Germany) after wet digestion through high-quality grade (Suprapur® Merk, Darmstadt, Germany)

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mineral acids and oxidants (HNO3 and H2O2) following previously described protocols (Squadrone

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et al., 2016). The analytical methods were validated according to UNI CEI EN ISO/IEC 17025

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(General Requirements for the Competence of Testing and Calibration Laboratories). The limit of

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quantitation was 0.010 mg Kg-1 for all the analysed elements and all concentrations are given on a

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wet weight basis.

178 2.3. Data analysis

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The range, mean, median and standard deviation of metal concentrations of each pool are reported

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in Table 2. For each element, ANOVA and Bonferroni’s test were applied to evaluate whether there

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were significant differences between the groups of samples from the different areas, and to assess

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the differences between three different types of marine environment (open waters, lagoon and

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harbour). The harbour of Porto Garibaldi was excluded from the final analysis because it is directly

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connected to the Comacchio Lagoon and not an enclosed area. Results with a p-value Fe (80.00) > Cu (76.95) > Al (38.45) > Mn (9.50) > As (3.5) > Se (0.89)

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> Cd (0.23) > Pb (0.195) > Ni (0.20) > Cr (0.195) > Sn (0.06) > Hg (0.02), and Tl (0.6; P < 0.05). Interestingly, Cd and Hg appeared to be negatively correlated (r >0.5; P < 0.05).

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3.4. Maximum number for safe consumption

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The number of oysters required to exceed the safety limits are reported in Table 4. The Sn

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concentrations were very low and this element was excluded from the analysis.

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4. Discussion 11

ACCEPTED MANUSCRIPT 4.1. Trace metals in relation to environmental conditions

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The Adriatic, especially its northern area, is strongly influenced by the freshwater input from large

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rivers, acting on salinity and trophic condition, in particular. Then, the geographic distribution of

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contaminants of inland origin is influenced by both the main anticlocking current and the

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anemometric conditions (Figure 1). A large data set shows that a positive gradient of Hg

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concentration in sediments from the southern to the northern Adriatic exists (Ferrara and Maserti,

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1992), and the results of the present study in oyster soft tissues support the existence of this

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phenomenon. However, we only partially observed the regional dynamics of dispersion Covelli et

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al. (2001) reported for the Gulf of Trieste. Isonzo River was once considered as the primary source

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of Hg pollution in the Gulf of Trieste (Horvat et al., 1999), with higher concentrations near the river

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mouth and an evident transport of mercury in a northern, especially in a northwestern, direction

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respect to a southern direction. However, we detected higher Hg levels in the samples collected

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from Muggia than Monfalcone. This difference may have been due to an additional and unknown

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pollution source in the southern part of the Gulf. Our observation of higher Hg concentrations in the

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samples from Cavallino-Treporti and Marano are shared by the findings of mercury contamination

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reported by Piani et al., 2005. The inputs of Hg in the Marano and Venice Lagoons, derived from

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chlor-alkali discharges from industrial plants, resulted in comparable levels of contamination. Part

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of this contamination may also be associated with the inputs from the Isonzo River through a

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westward long-range transport of fine particles with organically bound Hg forms (Biester et al.,

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2000). A similar situation was observed in the Orbetello Lagoon, where regional natural

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contamination (Romano et al., 2015) is reflected by the Hg bioaccumulation in oysters. Indeed,

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according to Lacerda and Gonçalves (2001) and Han et al. (2007), wetlands and coastal lagoons are

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important areas for Hg methylation, which improves the bioavailability of this element. This

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explains the significant higher Hg concentration observed in lagoons. The Hg levels in the samples

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from the Varano Lagoon suggest that Hg contamination in this region is absent. Interestingly,

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ACCEPTED MANUSCRIPT although the study conducted by Fabbri et al. (2001) found the Po River mouth and the Ravenna

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Lagoon to be highly polluted areas, the Hg levels we detected in the samples from the Caleri

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Lagoon, Porto Garibaldi and Cervia were all very low.

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The cadmium uptake depends on its chemical speciation, cadmium ion Cd2+ being more

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bioavailable, and it is mainly influenced by water salinity (De Lisle et al., 1988; De Wolf et al.,

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2004) and by the presence of organic ligands in water (Blust et al., 1995). We observed that

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individuals collected from lagoons contained, on average, three times less cadmium than those from

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open waters, indicating a negative correlation between Cd and Hg. Several environmental factors

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differentiate the Orbetello Lagoon from the northern Adriatic lagoons; nonetheless, the comparable

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levels of Cd detected in these enclosed areas may be imputable to common characteristics induced

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by high trophic conditions and the presence of shallow waters. Interestingly, the Cd content in

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individuals from the Varano Lagoon was similar to or slightly higher than those collected from open

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waters. A study carried out during the summer of 2000 (Spagnoli et al., 2002) reported moderate Cd

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concentrations in the sediments of the lagoon. The reason for the high levels we detected is still

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unclear. Several causative hypotheses may be advanced: an unknown source of contamination or

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some peculiar environmental conditions with respect to other lagoons or effluents from agriculture.

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As regards this last factor, a high correlation has been demonstrated between the concentrations of

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Cd and plant nutrients such as phosphates and nitrates in waters (Bewers et al., 1987).

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In marine environments, lead exhibits a high affinity towards organic substances and clay minerals,

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resulting in a preponderance of the sediment-bound form. Low Pb concentrations are usually

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present in shellfish because of the limited bioavailability of both dissolved and dietary lead to

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marine animals (Amiard et al., 1985). The median Pb levels we detected are comparable to the

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value of 0.131 mg.kg-1 in Pacific oysters reported in a previous study carried out in the Ligurian Sea

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(Squadrone et al., 2016), but the concentrations in the samples from Giulianova, and even more so

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in those from Muggia, were significantly higher than the median value. Differently from the high

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ACCEPTED MANUSCRIPT concentration of Pb in sediments in the Varano Lagoon observed by Spagnoli et al. (2002) between

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1999 and 2000, we did not detect high Pb levels in the oysters collected from this site. The positive

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correlation between Pb, Cu, and Sn, and between Sn and Zn could be related to the harbour

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environment. In fact, the high concentration of Cu in harbours is known to result from the use of

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antifouling paints for vessel hulls, while the presence of Pb probably derives from fuel discharges.

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Although regulations on the use of Sn in antifouling paints went into effect in the EU in 1991 and

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its use was finally prohibited with European Regulation 782/2003, the Sn levels in the samples from

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Giulianova harbour were much higher than in those collected from the other sites. This port is an

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enclosed basin with scarce water exchange, which could explain the high concentrations we

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observed. In contrast, the harbour of Porto Garibaldi is a canal connecting the Comacchio Lagoon to

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the open sea and it did not show this port-related pollution. Although located on the southern side of

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the Gulf of Trieste, the Muggia sampling site shares similar characteristics with the harbour of

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Giulianova, and the samples from Muggia contained high concentrations of the three elements Cu,

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Pb, and Sn.

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Arsenic is widely distributed throughout the marine environment and is characterized by a complex

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cycle. Because its accumulation in animals seems to be promoted by a benthonic lifestyle and a

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close relationship with sediments (Wu et al., 2014), high As levels may be detected in bivalves in a

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contaminated environment. The median As concentration (3.5 mg kg-1 w.w.) we found was twice as

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high as the value Squadrone et al. (2016) reported in C. gigas from the Ligurian Sea, but it was very

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close to the concentration observed in European flat oysters from the Croatian coasts of the Adriatic

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(Bilandžić et al., 2016). The high As concentration found in the Orbetello Lagoon was consistent

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with the results obtained by Romano et al. (2015). As pointed out for Hg, the main source of As

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contamination is probably related to the basin’s geochemical characteristics, but a contribution from

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the industrial and agricultural chemical wastes could not be excluded.

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Cu, Fe, and Zn are three elements essential to life, and the high ability of Pacific oyster to

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ACCEPTED MANUSCRIPT concentrate these metals (Funes et al., 2006, Pan and Wang 2009) was noted in the present study,

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with high concentrations detected in samples from all sites. These bivalves also accumulated high

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quantities of Al, a non-essential element. Cu can be considered a port-related contaminant, and

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CuO2, the main biocidal compound of antifouling paints, is often associated with Zn to improve its

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efficiency (Guardiola et al., 2012). The source of the high concentrations of Fe and Zn found in the

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samples from Cavallino-Treporti could also be related to the pollution from the Marghera industrial

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area, such as observed in sediments by Bellucci et al. (2002).

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The other essential elements, Cr, Ni, and Se, were present in low concentrations. The Muggia site is

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characterized by multifactorial pollution with Hg and port-related metals (As, Cr, Ni, Se, and Zn) at

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the same time. This difference could be explained by the long-standing presence of industry, port

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activities, and oil unloading around Trieste. Moreover, because the Bay of Muggia has a reduced

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hydrodynamism, the high concentrations of Cu, Pb, and Zn in the samples from this site reflected

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the storage of these elements in the bay sediments. However, the lack of previous data on metal

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concentrations in oysters precluded detailed assessment of the trend of contamination in this area.

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Unexpectedly, the Mn concentration in the samples from Muggia was considerably lower than the

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levels detected in the samples from the other sites.

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Generally, the values of the trace element levels measured during the present study are partially

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shared by previous investigations, for instance, those conducted in the Ligurian Sea (Squadrone et

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al., 2016) or in the native range of the species such as the Korea Strait (Mok et al., 2015). Except

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for Al, Pb, Cr, and Hg, the trace element levels reported by Squadrone et al. (2016) were lower than

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those we detected. This difference may have been due to the different sampling seasons and the

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physiological status of oysters. In the present study, the sampling took place during the pre-

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spawning period (spring), when the concentration of trace elements detectable in mollusc tissues is

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supposed to be highest (Najdek and Sapunar, 1987; Claisse, 1992), if compared to late summer and

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early autumn, when minimal concentrations are observed. Although bivalves and oysters in

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ACCEPTED MANUSCRIPT particular, are good bioindicators, the seasonal fluctuation of trace element concentrations linked to

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reproductive cycles is a drawback to their use because it complicates the comparison of data.

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However, because triploid specimens of Pacific oyster are available from hatcheries, and because

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they are characterized by the inhibition of gametogenesis, they are less subject to seasonal changes

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than diploid individuals of other bivalves, making them more suitable for biomonitoring campaigns.

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4.2. Human exposure to harmful elements and environmental suitability for oyster farming

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Oysters are edible marine organisms of commercial value worldwide; therefore, it is of primary

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importance to assess whether there is a risk associated with their consumption due to trace element

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concentrations in their tissues. Several studies (Eisler et al., 1972) have found that they have a

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greater capacity to accumulate Cd, but also Cu, Fe, and Zn, than other bivalve species such as clams

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(Baudrimont et al., 2005), mussels (Shulkin et al., 2003; Squadrone et al., 2016) or scallops (Mok et

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al., 2014). Szefer et al. (1999) and Soto-Jiménez et al. (2001) demonstrated that the concentrations

389

of these four elements detected in the soft tissues of oysters and in the sediments are related by a

390

biota-sediment accumulation factor (BSAF) (Arnot and Gobas, 2006) of 60, 48, 8, and 5,

391

respectively, while Dominik et al. (2014) reported a BSAF of 0.36 for Hg.

392

With regard to European Regulations, the concentrations of Hg and Pb in all the 72 pooled samples

393

from sites along the Italian coasts were below the current maximum limits set by the European

394

Commission to safeguard human health. The only exception was the Cd level in one pooled sample

395

from Capoiale-Varano, very close to the legal limit of 1 mg kg-1 w.w. It is a non-essential metal,

396

highly toxic for humans, and probably carcinogen (IARC, 1993; Bernard A., 2008). Cd affects

397

typically the kidneys, by involving the proximal tubular cells that may lead to renal failure, and

398

bones by inducing osteoporosis (Jarups et al., 1998; EFSA, 2012). However, N resulted reasonably

399

high. Obviously, this value is estimated without taking into account additional intakes of cadmium

400

from the diet. High Cd levels could also influence the zootechnical performances in aquatic

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ACCEPTED MANUSCRIPT animals, interfering with biologic mechanisms, as observed in oysters (Sokolova et al., 2004),

402

mussels (Viarengo et al., 1994), sponges (Müller et al., 1998), sea urchins (Roccheri and Matranga,

403

2010), crustaceans (Verriopoulos and Moriatou-Apostolopoulou, 1981), and fish (Voyer et al.,

404

1979). In invertebrates, cadmium induces changes in tissue organization, immune response, and

405

gene expression (Chiarelli and Roccheri, 2014). It has been shown in C. virginica that cadmium

406

induces haemocyte apoptosis (Sokolova et al., 2004).

407

In the samples collected during this study, the Hg levels were low, also in the specimens from

408

polluted areas, probably due to their low-trophic level. Mercury has highly toxic effects on the

409

environment and human health, especially its methylated form methylmercury (CH3Hg) which

410

tends to bio-accumulate and bio-magnify in biota throughout the aquatic food chain (May et al.,

411

1987). The toxicity of mercury and mercury compounds for marine fauna has been demonstrated by

412

several studies (Liu et al., 2011; Longo et al., 2013; Singaram et al., 2013).

413

The sampling site of Muggia showed high concentrations of lead. If humans and animals ingest lead

414

over tolerable limits, it can damage the nervous system (Nava-Ruiz et al., 2012, WHO, 2015) and it

415

can easily cross the placental barrier (Goyer, 1995). There is no current PTI for Pb, however. Lead

416

causes also irregular early development in invertebrates (Tellis et al., 2014) and biochemical and

417

histological toxic effects (Hariharan et al., 2014) that may penalise the growing performances

418

during farming.

419

Arsenic chemical forms, including both inorganic and organic compounds, have extremely variable

420

toxicological effects. The non-toxic organic compounds, such as methylated arsenicals,

421

arsenocholine, arsenobetaine, arseno-sugars, and arseno-lipids (Gebel, 2001), are the predominant

422

forms present in marine animal tissues (Phillips, 1990; Francesconi et al., 1998). These compounds

423

are thought to be the final products of detoxification processes and are easily eliminated by animals

424

and humans (Kaise et al., 1985). Some exceptions aside (Phillips and Depledge, 1986; Fattorini et

425

al., 2004), these organic forms generally present in the majority of seafood such as bivalves

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17

ACCEPTED MANUSCRIPT contribute to the low toxicity of these foodstuffs. However, the toxicity of soluble inorganic arsenic

427

has repercussions on marine biota, though the sensitivity depends on species and other

428

environmental factors (Sanders and Vermersch, 1982; Phillips, 1990).

429

Tin and aluminium are non-essential elements for humans. The Sn levels we detected in the samples

430

from all the sampling sites were too low to represent a danger for human health. Nonetheless, a

431

trace presence of Sn in water

Trace element occurrence in the Pacific oyster Crassostrea gigas from coastal marine ecosystems in Italy.

The Pacific oyster is one of the world's most widespread bivalves and a suitable species for biomonitoring trace elements in marine environments thank...
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