Geochemical survey and metal bioaccumulation of three bivalve species (Crassostrea gigas, Cerastoderma edule and Ruditapes philippinarum) in the Nord Médoc salt marshes (Gironde estuary, France)

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Abstract

A 15-month experiment combining a geochemical survey of Cd, Cu, Zn and Hg with a bioaccumulation study for three filter-feeding bivalve species (oysters, Crassostrea gigas; cockles, Cerastoderma edule; and clams, Ruditapes philippinarum) was conducted in a breeding basin of the Nord Médoc salt marshes connected to the Gironde estuary, which is affected by historic polymetallic pollution. Regular manual surface measurements of temperature, salinity, pH and dissolved O2 concentration and hourly multiprobe in situ measurements throughout several periods for 6–8 weeks were performed. The geochemical behavior of metals in water, suspended particulate matter and sediment and their ecotoxicological impact on the three bivalve species were evaluated by in situ exposure of juvenile oysters (water column) and adult cockles and clams (sediment surface).

The physico-chemical parameters reflected seasonal variations and basin management. A distinct daily periodicity (except salinity) indicated intense photosynthesis and respiration. In summer, low dissolved O2 saturations (∼40–50%) occurred in the early morning at 30 cm above the sediment, whereas in depressions, the water column near the sediment surface was suboxic. Cadmium, Zn and Cu concentrations in suspended particulate matter exceeded typical estuarine values and were much higher than the homogeneously distributed concentrations in different depth ranges of the basin sediment. Particles collected in sediment traps showed intermediate metal concentrations close to sediment values. These results suggest trace metal recycling due to reductive dissolution under suboxic conditions at the sediment surface resulting in trace metal release to the water column and adsorption onto suspended particles. Dissolved Cd, Zn and Hg concentrations (e.g. 13–136 ng l−1; 0.3–25.1 μg l−1 and 0.5–2.0 ng l−1, respectively) in the basin corresponded to the concentration range typically observed in the Gironde estuary, except for some maximum values attributed to metal recycling. In contrast, dissolved Cu concentrations (1.08–6.08 μg l−1) were mostly higher than typical estuarine values, probably due to recycled Cu complexation by dissolved organic matter. Growth, bioaccumulation rates and kinetics in the whole soft body of the bivalves were analyzed every 40 days. Although Cd bioaccumulation of oysters was lower in the basin than in the estuary during the same period (27,000 ng g−1, dry weight and 40,000 ng g−1, respectively) these values are largely above the new human consumption safety level (5000 ng g−1, dw; European Community, 2002). For cockles and clams, Cd bioaccumulation was lower, reaching 1400 ng g−1 and 950 ng g−1, respectively. Similar results were obtained for Zn and Cu suggesting physiological differences between the species and/or differences in the exposure of the organisms due to physico-chemical conditions and metal distribution between dissolved and particulate phases. In contrast, Hg bioaccumulation was highest for cockles reaching bioconcentration factors of ∼200,000, which even exceeded that of Cd in oysters (50,000) for the same exposition period. Nevertheless, Hg concentrations remained relatively low in the three bivalve species.

Introduction

The Gironde estuary (southwestern France) is characterized by a historic cadmium (Cd) contamination of the water and the sediment, which originated from a former ore treatment plant in the industrial basin of Decazeville (Latouche, 1988, Jouanneau et al., 1990; Fig. 1). The Cd pollution was discovered in the early 1980s by the National Observation Network (RNO), as the Cd concentrations measured in oysters from the Gironde estuary were close to 100,000 ng g−1 (dry weight). This value represents 20 times the consumption safety level currently authorized in France for marine bivalves (5000 ng g−1, dry weight or 1000 ng g−1 fresh weight; CE No. 466/2001; Boutier et al., 1989, Latouche, 1992). As a consequence, the Gironde estuary has been classified as “zone D”, i.e. interdiction of oyster recovery for consumption, production or purification. After an accidental polymetallic pollution (Cd, Zn, Cu, Hg, Ba, As) in 1986, important work was done (e.g. groundwater treatment) limiting Cd emission into the Lot River (Roux and Simonet, 1987, Blanc et al., 1999, Audry et al., 2003). After a distinct decrease of Cd emission in the early 1990s, Cd transport in the Lot–Garonne River system, still accounts for 40–80% of the annual gross fluxes into the Gironde estuary (Schäfer et al., 2002, Blanc et al., 2004, Audry et al., 2004). Important sediment stocks (9.47±0.9 106 m3; ∼200 t of Cd; Lapaquellerie et al., 1995) accumulated in the Lot valley between the Riou-Mort and the Garonne River (Fig. 1) may represent additional Cd sources due to remobilization by floods or dredging (Blanc et al., 1999, Audry et al., 2004). Although Cd is mainly transported in the particulate phase, most of it (∼90%) becomes highly bioavailable by dissolution due to estuarine biogeochemical processes and management (e.g. Elbaz-Poulichet et al., 1996, Kraepiel et al., 1997, Robert et al., 2004). As a result, Cd concentrations in the Gironde's oysters show a progressive decrease of 30–40% between 1979 and 1993 (e.g. Jouanneau et al., 1990, Michel et al., 2000), but average values remain very high (National Observation Network—RNO, France).

During the past 15 years, several fish farms have developed production of kuruma prawn (Penaeus japonicus) in the Nord Médoc salt marshes, adjacent to the Gironde estuary (Fig. 1). In these breeding basins, periodically alimented by water from the Gironde estuary, an important proliferation of savage cockles (Cerastoderma edule) of economic interest was observed each year. Filter-feeding bivalves filter large quantities of water, resulting in bioaccumulation of ambient metals (Andrès et al., 1999, Baudrimont et al., 2003, Hamza-Chaffai et al., 2000).

The aim of the present 15-month survey (May 2000 to December 2001) in a Nord Médoc breeding basin under realistic conditions, was to characterize the geochemical behavior and ecotoxicological impact of selected heavy metals (Cd, Cu, Zn and Hg) on three bivalves of economical interest (Crassostrea gigas, Cerastoderma edule and Ruditapes philippinarum). The impact of physico-chemical conditions and heavy metal contamination levels in water, suspended particulate matter (SPM) and sediment on bioaccumulation rates and kinetics is analyzed and discussed.

Section snippets

Study site

The present large-scale experimentation was conducted in one of the breeding basins of the “Bleu Médoc” fish farm at St Vivien de Médoc, France. The farm consists of 11 basins (each of 2.3 ha of surface and ∼0.8 m depth), which were dredged 30 years ago (Fig. 1). The main activity of this farm is kuruma prawn (P. japonicus) production. The basins are directly supplied by the Gironde estuary waters via a small channel, controlled by a gate. During the 15-month experiment, the water in the basin

Physico-chemical parameters

Temperatures measured throughout the experiment reached maximum values of 28 °C in summer and minimum values of 5 °C in winter. There were no systematic differences between temperatures obtained by the multiprobe and manual measurements (Fig. 2). Salinity also showed seasonal trends with maximum values of S=25 at the end of summer and minimum values of S=10 in winter. From July to September 2000 salinities were systematically higher (up to 3 points) at ∼50 cm depth than in surface water (Fig. 2

Geochemical scenario

Variation of physico-chemical parameters throughout the experiment reflects seasonal changes and basin management. Temperature reflects length and intensity of exposition to sunlight at both, seasonal and daily time-scale (Fig. 2, Fig. 3). Additionally, rapid decreases in temperature and salinity are due to important precipitation, i.e. dilution by rainwater. In contrast, decreasing temperature coinciding with increasing salinity was due to basin alimentation by estuarine water. On a seasonal

Conclusion

The present study was part of a larger research program realized in four basins on three aquaculture farms in the Nord Médoc salt marshes, to evaluate the impact of geochemical conditions on metal bioaccumulation by shellfish under realistic conditions of prawn production. The basin presented in this work corresponded to the reference site without perturbations by prawn production. The results show the high potential of Cd, Cu and Zn bioaccumulation in oysters, compared to other species and

Acknowledgements

The authors wish to thank Y. Lapaquellerie, N. Maillet, H. Bouillard, V. Roques-Duflo, G. Durrieu, G. Lavaux, E. Maneux, A. Palvadeau and B. Etcheverria for their important support in field work, analysis and data treatment. We thank also the Bleu Médoc fish farm for their important contribution. This work is part of the GIS ECOBAG program and was financially supported by the Agence de l'Eau Adour-Garonne, Conseil Général de la Gironde, the European Community (FEDER-PESCA), District de la

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