Elsevier

Science of The Total Environment

Volume 532, 1 November 2015, Pages 184-194
Science of The Total Environment

A multitracer approach to assess the spatial contamination pattern of hake (Merluccius merluccius) in the French Mediterranean

https://doi.org/10.1016/j.scitotenv.2015.06.020Get rights and content

Highlights

  • Hg and PCB concentrations were assessed in French Mediterranean hake.

  • Stable isotope and otolith shape analyses were used in combination.

  • Local isotopic and contamination patterns were observed.

  • Hg values were high in Corsica, PCB in the Gulf of Lions.

  • Combined ecotracers are powerful to discriminate between local populations.

Abstract

Chemical contamination levels and stable isotope ratios provide integrated information about contaminant exposure, trophic position and also biological and environmental influences on marine organisms. By combining these approaches with otolith shape analyses, the aim of the present study was to document the spatial variability of Hg and PCB contamination of the European hake (Merluccius merluccius) in the French Mediterranean, hypothesizing that local contaminant sources, environmental conditions and biological specificities lead to site-specific contamination patterns. High Hg concentrations discriminated Corsica (average: 1.36 ± 0.80 μg g 1 dm) from the Gulf of Lions (average values < 0.5 μg g 1 dm), where Rhône River input caused high PCB burdens. CB 153 average concentrations ranged between 4.00 ± 0.64 and 18.39 ± 12.38 ng g 1 dm in the Gulf of Lions, whatever the sex of the individuals, whereas the highest values in Corsica were 6.75 ± 4.22 ng g 1 dm. Otolith shape discriminated juveniles and adults, due to their different habitats. The use of combined ecotracers was revealed as a powerful tool to discriminate between fish populations at large and small spatial scale, and to enable understanding of the environmental and biological influences on contamination patterns.

Introduction

The release of chemical contaminants in the marine environment is one of the main threats currently altering marine individuals, populations and ecosystems (Fitzgerald and Clarkson, 1991, Fleeger et al., 2003, Halpern et al., 2008, Tartu et al., 2013). This issue is of particular concern in the Mediterranean Sea, as the numerous highly-populated and industrialized countries around this sea exert a strong pressure on it (Durrieu de Madron et al., 2011). Among all contaminants, mercury (Hg) and polychlorobiphenyls (PCB) are of particular concern. Mercury is emitted in the environment as a volatile metal (Hg0) of both natural and anthropogenic origins, with a three-fold increase in anthropic emissions since the industrial era (Streets et al., 2011, UNEP, 2013, Lamborg et al., 2014). After deposition, as HgII, Hg is transformed by bacteria into methylmercury (MeHg), its bioamplifiable and toxic form. The case of Hg is peculiar in the Mediterranean, as biogeochemical and biological features of this sea cause the “Mediterranean mercury anomaly”, i.e. higher Hg concentrations in Mediterranean organisms than in conspecifics from other environments, whereas Hg concentrations in water or sediment do not differ (Aston and Fowler, 1985, Cossa and Coquery, 2005, Cossa et al., 2009, Cossa et al., 2012, Harmelin-Vivien et al., 2009, Heimbürger et al., 2010). Polychlorinated biphenyls (PCBs) are a group of synthetic organochlorinated compounds which have been produced as commercial technical mixtures since the 1920s. They have been used in a wide range of applications, such as coatings, inks, flame retardants and paints, but their major applications were in electric appliances, heat transfer systems and hydraulic fluids. PCB open applications were banned in many countries in the 1970s but remained in use in closed systems (such as capacitors and transformers) before a complete ban in the 1990s. However, their high lipophilicity and environmental stability make them persist in the environment for long periods, resulting in a wide geographical distribution. These compounds are considered among the most dangerous pollutants because of their toxicity (Ahlborg and Hanberg, 1994, Loonen et al., 1996) stability, long biological half-life, and high liposolubility. A decrease of PCB concentrations in biota is thus currently expected (Aguilar and Borrell, 2005), but few long-term studies are available to document this trend. Both MeHg and PCBs are bioaccumulable and biomagnifiable along food chains, with a potential risk for high trophic level predators (Borgå et al., 2001, Fisk et al., 2001, Nfon and Cousins, 2006).

Since consuming contaminated marine products is the main source of human contamination (Fitzgerald and Clarkson, 1991, Endo et al., 2013), most studies were dedicated to assessing this risk, by documenting crude Hg or PCB levels in marine products, with little interest in the underlying biological or environmental processes (e.g. Bocio et al., 2007, Storelli, 2008, Storelli and Barone, 2013). Chemical contaminants emerged recently as useful ecotracers of trophic patterns or environmental parameters when used in combination with other tools, mostly stable isotope analyses (Fisk et al., 2002, Chouvelon et al., 2014, Cresson et al., 2014, Brown et al., 2015, Lavoie et al., 2015). This combined approach has become classical, since the C and N stable isotope ratio or the contaminant level of a fish is dependent upon its diet and the two techniques provide complementary time- and space-integrated information about trophic patterns. The nitrogen isotopic ratio and contaminant burden increase with trophic level providing combined information about the position of an organism in the trophic web. In a similar way, contaminant analyses can discriminate between two organic matter (OM) sources with similar isotopic ratios but different contamination levels (Cresson et al., 2014, McMeans et al., 2014). Finally, contamination levels and stable isotope ratios are under the control of different metabolic and environmental processes, such as local contamination source, growth rate or primary production intensity (Fisk et al., 2001, Fisk et al., 2002, Hoekstra et al., 2003, Bodiguel et al., 2009a, Bodiguel et al., 2009b, Dierking et al., 2009, Cossa et al., 2012, Harmelin-Vivien et al., 2012a). Combining the results provided by these techniques was thus recently used as an effective tool to discriminate between different local populations influenced by different environmental conditions or contaminant sources (Carravieri et al., 2014, Chouvelon et al., 2014, Brown et al., 2015, Lavoie et al., 2015). In a similar way, analyzing the shape of otoliths provides information about the local environmental conditions. Otoliths (“earstones”) are calcified pieces of the inner ear of teleosts (ray-finned fishes), the general shape of which is species-dependent. At a fine scale, within-species variation of the shape can reveal the influence of environmental parameters such as temperature and/or food availability (Lombarte and Lleonart, 1993, Gagliano and McCormick, 2004, Mérigot et al., 2007, Morat et al., 2012b). Despite being a promising approach, otolith shape, contaminant, and stable isotope analyses have not to date been used in combination.

In the French Mediterranean, the Gulf of Lions is an area of great ecological and economic importance but also of great concern, and under the major influence of the Rhône River. On the one hand, the Rhone River watershed is highly populated and industrialized, and the river is an important source of contaminants to the Gulf of Lions (Miralles et al., 2006, Radakovitch et al., 2008, Cossa et al., 2014, Mourier et al., 2014). The Rhone River is considered notably as an important source of PCB, due to the heavy historical contamination of the river's sediments by chemical industry wastes (Durrieu de Madron et al., 2011, Mourier et al., 2014). On the other hand, the Rhône River runoff is the main source of OM in the Gulf of Lions, enhancing the biomass production of harvested fish species (Salen-Picard et al., 2002). More than 90% of the French Mediterranean fisheries are located in the Gulf of Lions, with European hake (Merluccius merluccius Linnaeus, 1758) being the most important species (Aldebert et al., 1993, Bănaru et al., 2013). In the 1990s, the French fleet trawled 2220 metric tons (t) of hake annually (Aldebert et al., 1993). Nowadays, these catches range between 780 and 1 500 t (Ifremer Fisheries Information System, P. Lespagnol, pers. comm.). Captures are mostly composed of juvenile individuals (13–14 cm) trawled on the continental shelf, as adult individuals migrate to deeper zones (up to 800 m depth) when growing (Recasens et al., 1998, Maynou et al., 2003). Since their growth rate is slower (De Pontual et al., 2006, Mellon-Duval et al., 2010), males stay longer on the shelf, and are predominantly harvested, which explains the imbalanced sex-ratio and the predominance of female hake in the Gulf of Lions. The high trophic position of hake and its predominance in Mediterranean fisheries (Aldebert et al., 1993, Harmelin-Vivien et al., 2012a, Sinopoli et al., 2012, Bănaru et al., 2013) have made necessary extensive assessment of the contamination patterns. Recent studies in the Gulf of Lions identify sex, growth rate, reproduction and diet as key factors to explain the contamination patterns (Bodiguel et al., 2009a, Bodiguel et al., 2009b, Mellon-Duval et al., 2010, Cossa et al., 2012, Harmelin-Vivien et al., 2012a). In particular, the lower burdens measured in females were explained by their faster growth which dilutes the contamination by a higher synthesis of tissues, and by the elimination of organic contaminants such as PCB during spawning (Bodiguel et al., 2009a).

Nevertheless, published studies have not investigated the spatial variation of PCB and Hg contamination in the French Mediterranean. In addition, the Hg and PCB concentrations in Corsican fish have been poorly investigated (Porte et al., 2002, Cresson et al., 2015). Consequently, the aims of the present study were to document the spatial contamination pattern in Mediterranean hake, with a special focus on Corsica, in order to investigate whether contamination patterns can be considered as site-specific, and if they can discriminate between local populations, as previously observed for other species or environments (Dierking et al., 2009, Chouvelon et al., 2014). The use of combined biomarkers would allow understanding of the relative importance of each marker to discriminate the influence of local contamination sources from environmental and biological features. Notably, ontogenetic shift of habitat and of diet, bioaccumulation of contaminants through fish lifespan, PCB inputs from the Rhône River in the Gulf of Lions and oligotrophy in Corsica would be expected to be major drivers of the contamination patterns.

Section snippets

Sampling sites

European hake (M. merluccius) individuals were collected by professional trawlers at three sites of the French Mediterranean (Fig. 1), two in the western part of the Gulf of Lions (Port la Nouvelle and Le Grau du Roi) and one in northeastern Corsica (Bastia). These sites were chosen on the basis of the hypothesis that they reflect different contamination levels. Port la Nouvelle is considered as a site far from major anthropic influences and low levels of contaminants were measured in biota in

Sample size, sex ratio and morphological indices

A total of 224 individuals were sampled (69 at Le Grau du Roi, 70 at Port la Nouvelle and 85 in Bastia). Average total length was close to 270 mm (Table 1) and not significantly different between sites (PERMANOVA F = 2.16, p = 0.12; Table S2). The sex ratio was largely imbalanced, with predominance of juvenile individuals in the smallest size-classes, and of females for larger individuals, consistently with the biology of the species. The pattern of length is nevertheless dependent on the sex and of

Discussion

Stable isotope ratios, contamination levels and otolith shape allowed a clear discrimination between hake in the Gulf of Lions and in Corsica. Since contamination is mainly driven by the diet (Hall et al., 1997, Cresson et al., 2014) and as Hg and PCB are biomagnified through the trophic network, determining accurately the diet and trophic position of fish is crucial to understanding contamination patters. Additionally, contamination patterns are also driven by local contamination sources, the

Acknowledgment

Thanks are expressed to our colleagues Benoit de Vogüe, Yoan Baldi and Serge Mortreux for their help with sampling, Patrick Lespagnol for hake landing statistics, Maryvonne Henry and Corine Tomasino for drawing of the map, and to the Companie Nationale du Rhône for Rhône river discharge data. Thanks are also expressed to the three fishermen for their participation in this project. Stable isotope analyses were performed at the LIENSs Laboratory, Université de la Rochelle by Gaël Guillou, Benoit

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