Biosphere Reserve of Camargue, France)

Environmental Pollution 157 (2009) 2493–2506 Contents lists available at ScienceDirect Environmental Pollution journal homepage: www.elsevier.com/locate/envpol Organochlorines in the Vaccare`s Lagoon trophic web (Biosphere Reserve of Camargue, France) H. Roche a,*, Y. Vollaire a, A. Persic a, A. Buet a, C. Oliveira-Ribeiro b, E. Coulet c, D. Banas a, F. Ramade a a Ecologie, Syste´matique et Evolution, UMR8079 CNRS, Universite´ Paris-Sud, AgroParisTech, F91405 Orsay Cedex, France b Departamento de Biologia Celular, Universidade Federal do Parana´, Caixa Postal 19031, CEP: 81.531-990, Curitiba, PR, Brazil c Nature Reserve of Camargue, La Capelie`re, F13200 Arles, France The Vaccare`s Lagoon trophic web biomagnifies organochlorine pollutants. article info abstract Article history: During a decade (1996–2006), ecotoxicological studies were carried out in biota of the Vaccare`s Lagoon Received 12 September 2008 (Biosphere Reserve in Rhone Delta, France). A multicontamination was shown at all levels of the trophic Received in revised form web due to a direct bioconcentration of chemical from the medium combined with a food transfer. Here, 27 February 2009 the pollutants investigated were organochlorines, among which many compounds banned or in the Accepted 6 March 2009 course of prohibition (or restriction) (PCB, lindane, pp0-DDE, dieldrin, aldrin, heptachlor, endosulfan.) and some substances likely still used in the Rhone River basin (diuron, fipronil). The results confirmed Keywords: the ubiquity of contamination. It proves to be chronic, variable and tends to regress; however contam- Organochlorines Aquatic trophic web ination levels depend on the trophic compartment. A biomagnification process was showed. Biosphere Reserve of Camargue A comparison of investigation methods used in other Mediterranean wetlands provides basis of Biomagnification discussion, and demonstrates the urgent need of modelling to assess the ecotoxicological risk in order to improve the management of such protected areas. Ó 2009 Elsevier Ltd. All rights reserved. 1. Introduction and the sedentariness of the organisms are prevailing factors, then the oldest individuals, which are usually the biggest ones, would be The inter-connections of wetlands with agricultural areas or the more contaminated. At the opposite, if pollutant discharges are other adjacent habitats lead subsequently to a chronic contami- accidental or occasional (field treatments, atmospheric drift, soil nation of aquatic ecosystems and their trophic webs. Due to their leaching, etc.), the ratio ‘exposed body surface’/‘body volume’ is position as sinks of wastewater from irrigation agriculture fields determining for the contamination level, since this ratio is gener- and run off, the Camargue wetlands are particularly endangered. ally higher in the smallest organisms (Randall et al., 1998; Fant and They receive residues of agrochemical sprayings, from continuous Reindelder, 2003; Xiulin and Zauke, 2004). According to this or intermittent inputs, likely transferred to the organisms during concept, within a food web, bioconcentration is higher at the low the bioaccumulation process (Albanis et al., 1996; van der Oost trophic levels (TLs) than in predators. This empirical theory, also et al., 1996; Mackay and Fraser, 2000; Weber and Goerke, 2003; suffers from exceptions due to the morphology and the surface Gewurtz et al., 2006). The qualitative and quantitative distribution structure of organisms (gill surface area in fishes, chitin in inver- of organic pollutants in the aquatic biota is largely dependent on tebrates, etc.). the solubility of the molecule in water or in lipids. Bioaccumulation Conversely, a trophic transfer leading to an increasing concen- proceeds overall in two ways: a direct transfer through the tegu- tration along a food chain is named the biomagnification process, ments (skin and gills) and/or by ingestion, or a transfer along the according to which the bioaccumulation is higher in a consumer food chain, from preys to predators. than in its food. Nevertheless, the two phenomena are often In a bioconcentration process, aquatic organisms retain and concomitant. Even if the high liposolubility of Persistent Organic concentrate chemical compounds from their environment Pollutants (POPs) renders such compounds more subject to (Ramade, 2007). When inputs are chronic and regular, the longevity biomagnification, their contamination ability in biota remains dependent on the physiological functions of species: i.e. assimila- tion, excretion and biodegradation. Biomagnification has been well * Corresponding author. Tel.: þ33 1 69 15 73 12; fax: þ33 1 69 15 56 96. described in long marine food chains (Wilson et al., 1995; Borga E-mail address: [email protected] (H. Roche). et al., 2001) or more generally in open ecosystems (Muir et al.,1996), 0269-7491/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2009.03.016 2494 H. Roche et al. / Environmental Pollution 157 (2009) 2493–2506 but, in shortest trophic webs composed of multi-food chains, the Beauchamp (2007) and at the opposite of a widespread idea, we demonstration is challenging (Kidd et al., 2001), as in Lake Erie virtually never observe any causal relationship between the lipid (Kwon et al., 2006) or in a coastal lagoon (Menone et al., 2000). contents of organisms and the concentrations of POPs, as Kucklick Due to its geographical location, in the centre of the Rhone delta, and Baker (1998) in the Lake Superior. Stable nitrogen isotope was the Biosphere Reserve of Camargue, and in spite of its multiple used as an indicator of trophic position (Minagawa and Wada,1984; statutes of protection (MAB–UNESCO), is exposed to random Vander Zanden and Rasmussen, 2001; McIntyre and Beauchamp, natural or anthropogenic disturbances, linked to a complex 2007) and biomagnification factors, adjusted for TL, were reported. hydrological system and human activities developed nearly. Among So, the present article is devoted to the synthesis of numerous them, the rice fields requires large volumes of water, so the Vac- results obtained during the last decade. Here, such a collection care` s Lagoon, the main water body of the Reserve, receives the provides the discussion basis about the trophic transfer of organ- effluents loaded with agrochemical products, as well as pesticides ochlorine contaminants in Mediterranean wetlands. coming from the Rhone River Valley. Since 1996, several research programs including biomonitoring, 2. Material and methods devoted to the study of aquatic organisms exposed to POPs, were carried out in the Vaccare`s Lagoon (Roche et al., 2000, 2002a,b). 2.1. Studied site Initially the projects were devoted to an ecotoxicological assess- The Reserve of Camargue-Rhone Delta nominated in 1977 by UNESCO as an ment in the eels (Oliveira Ribeiro et al., 2005, 2008; Buet et al., ‘International Reserve of Biosphere’ (position revised in 2006), ranks as the largest 2006). This common fish of Mediterranean coastal brackish protected coastal wetland in Mediterranean Europe (32 000 Ha.). As a deltaic wetlands fill all the required properties as a bioindicator species. complex of terrestrial, coastal and aquatic areas the Reserve displays a remarkable Nevertheless, its decline became alarming. Considering that the variety of natural habitat as well of plant and animal communities. Therefore, the Camargue Reserve stands as a major hot spot of Mediterranean coastal wetland observed contamination was obviously due to a long history of biodiversity. Here, attention was focused on aquatic species living in the brackish pesticide use with chemicals often banned (Roche et al., 2002a), our waters of the Vaccare`s Lagoon (43300 N4300 E), the largest water body of the researches have addressed the transfer of pollutants into the Reserve (6500 Ha) (Fig. 1). aquatic trophic web of the Vaccare`s water body. The contamination by pesticides and PCB in species sampled in spring and autumn 2.2. Organism sampling 2002 and 2005, were compared in this paper. The liposolubility of Eels were caught in spring and in autumn during a decade (1996–2005). The substances, characterized by their octanol-water partition coeffi- eels’ samples were divided into 4 stages of growth (juvenile, immature type 1, cient (log Kow) exceeding 5, would potentially generate a bio- immature type 2 and yellow eels). A total of 17 other aquatic species were sampled magnification process. However, as highlighted by McIntyre and from La Capelie`re site in the Vaccare`s Lagoon during 6 campaign experiments Fig. 1. The Rhone Delta, Biosphere Reserve of Camargue (France). H. Roche et al. / Environmental Pollution 157 (2009) 2493–2506 2495 P conducted in spring 2001, in autumn 2003 and in spring and autumn 2002 and Les Ulis France), first with hexane, to eluate DDT, HCB and PCB, then with hexane/ 2005. The studied organisms were zooplankton (copepods sp. þ larvae), Sphaeroma diethylether (90/10) for OCPs clean-up. sp, cokkles (Cerastoderma glaucum), mysids, gammarids (Gammarus salinus), pink The quantitative and qualitative analyses of organochlorine compounds were shrimps (Crangon crangon), brown shrimps (Palaemonetes varians), sand smelts achieved by gas chromatography with an AutoSystem XL (Perkin–Elmer), using ECD (Atherina boyeri), gobies (Pomatoschistus sp.), stickelbacks (Gastrosteus aculeatus), (electron capture detection) with an 63Ni Source and Nitrogen as make-up gas pipefish (Syngnatus acus), not to mention occasionally, common soles (Solea solea), according

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