3,3′-dichlorobiphenyl (non-Aroclor PCB-11) as a marker of non-legacy PCB contamination in marine species: comparison between Antarctic and Mediterranean bivalves
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).
Section snippets
Reagents and materials
All solvents were Super Purity Solvents (SpS™) and were supplied by Romil Ltd. (Cambridge, UK). To concentrate the extracts, nitrogen gas 5.0 (99.999%) was used. Isotope-labeled standard solution EC-4189-A was purchased from CIL (Cambridge Isotope Laboratories Inc., Tewksbury, MA, USA) and used as internal standard solution. Surrogate standard solution of PCB-11 was acquired from Dr. Ehrenstorfer GmbH (Augsburg, Germany). Standard reference materials (SRM, 1974C and SRM 2977: Mussel Tissue)
Results and discussion
The non-Aroclor congener PCB-11 was detected in all the samples regardless of the species analyzed and of the geographical areas of distribution. Furthermore, PCB-11 was one of the most abundant PCB congeners, representing on average 17.6% of total PCBs (126 Aroclor congeners plus PCB-11: Σ127PCBs) in Antarctic samples and the 15.6% in Mediterranean samples. Measured concentrations are reported in Table 1. As is frequently done in the literature, the percentage ratios of PCB-11 to Σ127PCBs and
Conclusions
The results of the present study clearly confirm the presence of non-legacy contamination by PCB-11 in the Antarctic environment, as shown by the not entirely negligible concentrations detected in specimens of A. colbecki collected at Terra Nova Bay (Ross Sea, northern Victoria Land). PCB-11 levels ranging between 0.25 and 36.49 ng g−1, on an average of 6.95 ng g−1 and the PCB-11/Σ7iPCBs percentage ratio is generally higher and more widespread than those observed in different Antarctic
Acknowledgments
This work was funded by the Italian Ministry of Education, Universities and Research (MIUR) through the project PRIN (Prot. 2010AXENJ8) and by the Italian National Antarctic Research Programme (PNRA; project number: 9.2). Sampling of mussels and clams was funded by the Veneto region (project code: 436/1/6/1686/2012). The authors want to thank Daniela Almansi for her accurate revision of the manuscript.
References (64)
- et al.
Polychlorinated dibenzo-p-dioxins and furans and non-ortho- and mono-ortho-chlorine substituted polychlorinated biphenyls in grey seals (Halichoerus grypus) from Sable Island, Nova Scotia, in 1995
Mar. Environ. Res.
(1999) - et al.
Growth, biochemical profile, and fatty acid composition of mussel (Mytilus galloprovincialis Lmk.) cultured in the open ocean of the Bay of Biscay (northern Spain)
Aquaculture
(2016) - et al.
PCBs in wild mussels (Mytilus galloprovincialis) from the N-NW Spanish coast: current levels and long-term trends during the period 1991-2009
Chemosphere
(2011) - et al.
Editorial – NOAA's Mussel Watch Program: incorporating contaminants of emerging concern (CECs) into a long-term monitoring program
Mar. Pollut. Bull.
(2014) - et al.
Possible influence of lipid content on levels of organochlorine compounds in mussels from Galicia coast (Northwestern, Spain). Spatial and temporal distribution patterns
Environ. Int.
(2004) - et al.
Role of filtering and biodeposition by Adamussium colbecki in circulation of organic matter in Terra Nova Bay (Ross sea, Antarctica)
J. Mar. Syst.
(1998) Industrial contaminants in Antarctic biota
J. Chromatogr. A
(2009)- et al.
The reproductive biology of the manila clam, Ruditapes philippinarum, from the north-West of Ireland
Aquaculture
(2006) - et al.
Chlorinated compounds and polybrominated diphenyl ethers (PBDEs) in mussels (Mytilus galloprovincialis) collected from Apulia Region coasts
Mar. Pollut. Bull.
(2013) - et al.
Recognizing different impacts of human and natural sources on the spatial distribution and temporal trends of PAHs and PCBs (including PCB-11) in sediments of the Nador Lagoon (Morocco)
Sci. Total Environ.
(2015)
QSAR approach to POPs screening for atmospheric persistence
Chemosphere
Gas-particle distributions, sources and health effects of polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs) and polychlorinated naphtalenes (PCNs) in Venice aerosols
Sci. Total Environ.
Retrospective biomonitoring of chemical contamination in the marine coastal environment of Terra Nova Bay (Ross Sea, Antarctica) by environmental specimen banking
Chemosphere
Age and productivity of the Antarctic scallop, Adamussium colbecki, in Terra Nova Bay (Ross sea, Antarctica)
J. Exp. Mar. Biol. Ecol.
PCB decomposition and formation in thermal treatment plant equipment
Chemosphere
Characterization and fingerprinting of PCBs in flue gas and ash from waste incineration and in technical mixtures
Chemosphere
Tracing the source of 3,3’-dichlorobiphenyl found in samples collected in and around Halifax Harbour
Mar. Pollut. Bull.
PCB dechlorination enhancement in Anacostia River sediment microcosms
Water Res.
Biodegradation of coplanar polychlorinated biphenyls by anaerobic microorganisms from estuarine sediments
Chemosphere
Is rain or snow a more efficient scavenger of organic chemicals?
Atmos. Environ.
Filtration rates of the Manila clam, Ruditapes philippinarum: dependence on prey items including bacteria and picocyanobacteria
J. Exp. Mar. Biol. Ecol.
Determination by HRGC/HRMS of PBDE levels in edible Mediterranean bivalves collected from north-western Adriatic coasts
Microchem. J.
Seasonal variations of susceptibility to oxidative stress in Adamussium colbecki, a key bioindicator species for the Antarctic marine environment
Sci. Total Environ.
Antarctic environmental Specimen Bank
Polycyclic aromatic hydrocarbons in surface seawater and in indigenous mussels (Mytilus galloprovincialis) from coastal areas of the Saronikos Gulf (Greece)
Estuar. Coast. Shelf Sci.
Persistent organic pollutants (POPs) in Antarctica: occurrence in continental and coastal surface snow
Microchem. J.
Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in Antarctic ice-free areas: influence of local sources on lakes and soils
Microchem. J.
Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals' pollution in coastal areas from the Saronikos Gulf of Greece
Mar. Pollut. Bull.
An overlooked environmental issue? A review of the inadvertent formation of PCB-11 and other PCB congeners and their occurrence in consumer products and in the environment
Sci. Total Environ.
Three-year atmospheric monitoring of organochlorine pesticides and polychlorinated biphenyls in Polar regions and South Pacific
Environ. Sci. Technol.
Analysis of Polychlorinated Biphenyls (PCB) by glass capillary gas chromatography – composition of technical aroclor- and clophen-pcb mixtures
Fresenius Z. Anal. Chem.
Ecology of the Circumpolar Antarctic Scallop, Adamussium Colbecki (Smith, 1902)
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