3,3′-dichlorobiphenyl (non-Aroclor PCB-11) as a marker of non-legacy PCB contamination in marine species: comparison between Antarctic and Mediterranean bivalves

Highlights

• PCB-11 occurs in bivalves from both Antarctic and Mediterranean coastal areas.

• PCB-11 represents on average 16–18% of the total PCBs (n = 127).

• The presence of PCB-11 in Antarctica is related both to local and distant sources.

• PCB-11/Σ₇iPCBs ratios are higher than those observed in various Antarctic matrices.

• In the Adriatic Sea the highest concentrations are due to industry and ship traffic.

Abstract

In this study the accumulation of the 3,3′-dichlorobiphenyl (PCB-11) in monitoring organisms from the Antarctic and Mediterranean coastal environments has been investigated. This lesser-known PCB congener, unrelated to the industrial use of commercial mixtures, continues to be generated and released into the environment mainly as an unintentional by-product of pigment manufacturing. Specimens of the filter-feeders Adamussium colbecki from Terra Nova Bay and of Mytilus galloprovincialis and Ruditapes philippinarum from the north-western Adriatic coasts were collected and analyzed for PCB-11 by Gas Chromatography coupled both to Low-Resolution and High-Resolution Mass Spectrometry (LRMS, HRMS). In order to assess the influence of PCB-11 with respect to the legacy contamination, 126 PCB congeners related to the Aroclor commercial mixtures were simultaneously analyzed.

PCB-11 was detected in all the samples, regardless of the species and of the geographical area, representing on average 17.6% and 15.6% of the total PCBs (n = 127) in Antarctic and Mediterranean samples, respectively. In the Adriatic area the highest concentrations were related to the influence of industrial activities or ship traffic, while the highest value found in Antarctic specimens, namely those collected in the austral summer 1997–1998, was ascribed to a local anthropogenic source. The occurrence of PCB-11 in the other samples from Terra Nova Bay may be related to Long-Range Atmospheric Transport (LRAT), facilitated by the higher volatility of the analyte compared to the heavier PCB congeners. Nevertheless, more in-depth studies are needed in order to evaluate the relative contribution of local and distant sources.

Introduction

Polychlorinated biphenyls (PCBs) are among the main classes of persistent organic pollutants (POPs), used world-wide, are globally distributed in every environmental compartment. The sources of PCB contamination are commonly associated to the industrial use of commercial mixtures, such as Aroclors, which were banned from production and distribution in the United States in the 1970s by the Toxic Substances Control Act (Erickson, 1997, TSCA, 1976). However, different sources of PCBs, unrelated to the commercial distribution of mixtures, have been recently identified. In particular, the congener 3,3′-dichlorobiphenyl (abbreviated to PCB-11 according to the scheme developed by Ballschmiter and Zell, 1980) has been considered as a marker of non-Aroclor PCB contamination in the environment (Grossman, 2013). High levels of PCB-11 were detected in organic dyes by Hu and Hornbuckle (2010), mostly in diarylide yellows made from azo- and phtalocyanine pigments. The authors also suggested potential mechanisms for the formation of PCB-11 as a by-product during the manufacturing process of phtalocyanine pigments. These pigments are widely used in common consumer goods, such as newspapers, magazines, plastic bags, packaging and printing inks. From these sources the non-legacy congener may be released in air, water and sediments (Guo et al., 2014, Rodenburg et al., 2010), also as a residue of municipal solid waste incineration (Ishikawa et al., 2007, Jansson et al., 2011).

As observed for other low-chlorinated congeners, PCB-11 has high volatility and persistency in air, therefore it is likely to be significantly subjected to Long-Range Atmospheric Transport (LRAT; Gramatica et al., 2001). Due to this behaviour, the non-Aroclor congener has been found in almost every environmental matrix worldwide, including the Polar regions (DRBC, 2003, Giuliani et al., 2015, Gregoris et al., 2014, Hu et al., 2008). An average concentration of 5.44 pg m⁻³ was detected during the three one-year periods of air sampling (2005–2007) at Ny-Ålesund (Spitsbergen Island, Svalbard, Norway; Baek et al., 2011). The same monitoring program was adopted by the authors at the Antarctic site of King George Island from 2005 to 2009, where the PCB-11 levels turned out to be quite high, with an average concentration of 60.3 pg m⁻³. More recent studies confirmed the presence of this non-Aroclor congener in the Antarctic area: concentrations ranging from 428 fg m⁻³ to 3.2 pg m⁻³ were measured in air samples from Terra Nova Bay (Piazza et al., 2013). Values of PCB-11 ranging from 10 to 34 pg L⁻¹ were detected in the surface snow samples from the East Antarctic plateau and from the coastal areas of northern Victoria Land, where PCB-11 was one of the most abundant PCB congeners (Vecchiato et al., 2015a).

Despite the concern and evidence about the global distribution of non-legacy POP contamination, these compounds were often neglected and the assessment of the PCBs pollution is mainly based on the target congeners (i.e., the so-called “Dutch seven” or PCB indicators). Moreover, little is known about the potential adverse health effects of PCB-11 and of its uptake throughout the food chain. In the literature no evidence regarding the biomagnification of this congener has been observed, although PCB-11 has been recently detected in human serum (Koh et al., 2015, Vorkamp, 2016). Previous studies showed the presence of PCB-11 in grey seals from Nova Scotia and mussels from Halifax Harbour, Canada (Addison et al., 1999, King et al., 2002) as well as in striped bass from New York State, USA (Bush et al., 1989), confirming the ubiquity of this non-Aroclor congener. Moreover, in the Plan for the Portland Harbor Superfund Site assessment promoted by the US Environmental Protection Agency (EPA), a more in-depth survey on PCB pollution was developed between 2003 and 2008, providing a large data collection available on the EPA STORET (Storage and Retrieval) database (http://www.epa.gov/storet). Nevertheless, to the best of our knowledge, no other evidence has been found regarding the presence of PCB-11 in marine biota, especially in remote regions.

Antarctica is supposed to be a pristine environment. POP pollution in this region is a consequence of LRAT from urban areas, but local impacts may occur from the research stations set on the coastal areas, and from the correlated human activities (Corsolini, 2009, Vecchiato et al., 2015b). Adamussium colbecki (Smith, 1902), one of the most common marine organisms on Antarctic coasts (Stockton, 1984), is a very useful tool to monitor POPs and other relevant trace pollutants (Magi et al., 2004, Grotti et al., 2016; this issue), which may be accumulated, as in different environment other bivalve species do. Bivalve species are well-known indicators of marine contamination in urban areas and allow the comparative study of sites with different anthropogenic impacts (Bricker et al., 2014, Vlahogianni et al., 2007). In particular, several studies on the Mediterranean region, focused on monitoring POPs, analyzed the most common edible mollusks Mytilus galloprovincialis (Lamarck, 1819) and Ruditapes philippinarum (Adams and Reeve, 1850; Bellas et al., 2011, Kožul et al., 2009, Pizzini et al., 2015, Valavanidis et al., 2008). However, the majority of the available data about the bioaccumulation of POPs in biota refers to legacy contamination.

The main purpose of this work is to investigate and quantify the concentration of the PCB-11 in the Antarctic scallop A. colbecki and to assess its suitability as an indicator of non-legacy PCB contamination. Moreover, the Mediterranean M. galloprovincialis and R. philippinarum were also studied in order to compare the PCB-11 concentrations in areas at high anthropogenic impact to those found in remote regions. The samples of A. colbecki were collected at Terra Nova Bay (Ross Sea, northern Victoria Land) and obtained by the Antarctic Environmental Specimen Bank (ESB, http://www.bcaa.unige.it), whereas those of Mediterranean bivalves were collected along the northern coasts of Adriatic Sea (Italy).