Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

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<ul><li><p>Baseline</p><p>Edited by Bruce J. Richardson</p><p>Methylmercury bioconcentration in muscle tissue of the Europeaneel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)</p><p>Ina Arleny a,b, Hele`ne Tabouret c, Pablo Rodriguez-Gonzalez a, Gilles Bareille a,Olivier F.X. Donard a, David Amouroux a,*</p><p>a Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, IPREM CNRS UMR 5254, Universite de Pau et des Pays de lAdour,</p><p>Helioparc, F-64053 Pau, Franceb Provincial Health Laboratory of Central Kalimantan, JI Let. Jend. Soeprato No1 Palangka Raya 73112, Kalimantan Tengah, Indonesia</p><p>c IFREMER, Laboratoire des Ressources Halieutiques dAquitaine, Technopole Izarbel, 64210 Bidart, France</p><p>The life history of the European eel (Anguilla anguilla)begins in the Sargasso Sea in the Atlantic Ocean whereLeptocephalus larvae drift with the gulf stream in orderto reach European coastal waters. After their metamorpho-sis into transparent juveniles (glass eels) and an acclima-tising phase in estuaries, they migrate upstream into riversto become yellow eels (the sub-adult stage). The yellow eelsspend between 2 and 20 years of their lifetime in freshwateruntil they change into silver eels (the adult stage) andnally migrate back to the Atlantic Ocean for spawning(Gomez-Mourelo, 2005). A. anguilla is thus an organismable to tolerate a wide range of environmental conditions,including variations in oxygen availability, dierent rangesof salinities and exposure to a variety of anthropogeniccompounds. In addition, it is a migratory, benthic andbenthivorous species at the top of the food chain and ischaracterised by a high fat content (&gt;30%). For all thesereasons A. anguilla can bioaccumulate a wide range of con-taminants and it has been widely employed as a bioindica-tor of pollution caused by metals (Batty et al., 1996; Has-Schon et al., 2006) and organic contaminants (Storelliet al., 2007; Yamaguchi et al., 2003).</p><p>The environmental and toxicological impact of Hg bio-accumulation in sh is related to the methylation of inor-</p><p>ganic mercury to form the more toxic methylmercury(MeHg) species. Fish tend to concentrate MeHg in theirtissues by a factor of 105107, leading to dangerous levelseven in areas with tolerable Hg concentrations (Masonet al., 1996). It has been reported that about 98% of theHg present in aquatic systems is immobilised in sediments(Stein et al., 1996) and that most of the MeHg is producedat the sediment water interface as a result of biotic orabiotic transformations caused by specic redox gradientsand bacterial activity (Gilmour and Henry, 1991). Accord-ingly, A. anguilla may be an eective biomagnicator andbioaccumulator of Hg due to its longevity during the con-tinental development phase in freshwaters (where it foragesand lives upwards of 15 years) and its position at the top ofthe food chain as a carnivorous species feeding on benthicfauna (Mancini et al., 2005).</p><p>The River Adour (located at the South West of France)has a length of 335 km, enters the Atlantic Ocean at 4330 0North latitude 132 0 West longitude and drains a largeagricultural area of 17,000 km2. The Adour estuary isaected by a dynamic macrotidal range (up to 70 kmupstream) and it is under strong anthropogenic pressuredue to urban, agricultural and industrial activities includ-ing tourism, sheries or recreational boating (Brunet andAstin, 1999). In the upstream estuarine zone, the river pre-sents large, at man-made modied oodplains (knownlocally as the Barthes) that constitute an area of15 km2, lying up to 2 km on both sides of the river. The</p><p>The objective of BASELINE is to publish short communications on different aspects of pollution of the marineenvironment. Only those papers which clearly identify the quality of the data will be considered for publication.Contributors to Baseline should refer to BaselineThe New Format and Content (Mar. Pollut. Bull. 42, 703704).</p><p>* Corresponding author. Tel.: +33 559 407 756; fax: +33 509 407 781.E-mail address: david.amouroux@univ-pau.fr (D. Amouroux).</p><p>www.elsevier.com/locate/marpolbul</p><p>Marine Pollution Bulletin 54 (2007) 10311071</p></li><li><p>Barthes are ooded twice a year and play a signicanthydraulic and hydrological role owing their high storagecapacity. Such capacity, together with the existence ofman-made dykes, aords ood protection to the regionand allows a signicant dilution of point discharges inthe area (Brunet and Astin, 2000). The Barthes is a naturalhabitat for A. Anguilla (Gomez-Mourelo, 2005) and itsexploitation constitutes the basis of the economy of thelocal professional shermen and hence plays an importanteconomic role in this region. However, A. Anguilla stockhas been reported to be in dangerous decline in all its geo-graphic life areas (Dekker, 2000; Feunteun, 2002).</p><p>Mercury speciation analyses in surface sediments ofmacrotidal estuaries and coastal systems from the RiverAdour have shown a moderate contamination of MeHgand inorganic mercury (Stoichev et al., 2004). Moreover,bioaccumulation and biomagnication of MeHg in the tro-phic network of benthic macrofauna from the Adour estu-ary and its adjacent coastal zone has been recentlyobserved (Monperrus et al., 2005). Thus, speciation analy-sis of mercury in A. Anguilla from the River Adour appearsto be necessary in order to ascertain the risk of transfer(generated by mercury biomagnication) to the higher lev-els of the food web, including human beings. A. anguillahas been used as a biomarker for the study of mercury con-tamination in many aquatic ecosystems (Batty et al., 1996;Burger et al., 2001; Edwards et al., 1999; Linde et al., 1999;Maes et al., 2005; Ribeiro et al., 2005). However, there hasbeen only one study providing information about theMeHg levels in eels, particularly in long-ned eels Anguilladieenbachii from New Zealand (Redmayne et al., 2000).</p><p>Therefore, this is the rst environmental study reportingHg speciation data from European eels. The aim of thepresent work was the determination of inorganic mercuryand MeHg levels in muscle tissues of A. anguilla fromtwo dierent aquatic ecosystems of the Adour estuary.</p><p>This study is part of a research program, Groupementde Recherche Adour (GDR Adour), involving several lab-oratories that investigate possible eects of contaminantson dynamic eel populations. During this program, the sam-pling strategy was dened by the LRHA (Laboratoire deRessources Halieutique dAquitaine) IFREMER (Insti-tute Francais pour lExploration de la Mer) according to,rst, various phases characterizing the annual biologicalcycle of A. anguilla (colonizationsedentarisationdown-stream migration) and second, the specic period of agri-cultural practice such as maize plantation, irrigation andpesticide treatment. According to this, three periods ofsampling corresponding approximately to the months ofApril, July and October were selected.</p><p>The mercury speciation data reported in the presentstudy are derived from eels caught from two sampling sites(Fig. 1): the downstream estuarine zone (Redon site) and acanal located upstream in the oodplains (Barthes) at SaintLaurent de Gosse, sampled in July and October 2005,respectively. The Redon site is located in the mixing zoneof the Adour estuary and, therefore, is under the inuenceof urban and industrial activities as well as physicochemicalprocesses caused by the mixing of river water and seawater.The sampling site located at Saint Laurent de Gosse is in thefreshwater tidal zone of the estuary and mostly subjectto agricultural activities developed within the Barthes</p><p>N</p><p>AtlanticOcean</p><p>Tarnos</p><p>Urt</p><p>Anglet</p><p>Bayonne</p><p>N</p><p>AtlanticOcean Saline zone</p><p>Nive River</p><p>Kp 135</p><p>Kp 110110Kp 110</p><p>120Kp</p><p>Adour River</p><p>Gaves RiversFluvial zone</p><p>ADOUR ESTUARY</p><p>AdourEstuary</p><p>4332N</p><p>4330N</p><p>4328N</p><p>130W 115W120W 110W125W</p><p>Downstream estuarine samplingsite (Redon zone)</p><p>Floodplain sampling site (Saint-Laurent de Gosse)</p><p>Fig. 1. Location of sampling areas in the lower estuary and upper estuary oodplain (Adour River, France).</p><p>1032 Baseline / Marine Pollution Bulletin 54 (2007) 10311071</p></li><li><p>catchments. It is also linked to the estuary only by valves,permitting at some point the input of uvial water.</p><p>A total of 22 yellow eel samples were analysed for Hgspeciation. Fifteen samples were collected from the down-stream estuarine zone (Redon site) and the rest from theupstream wetland of Barthes (Saint Laurent de Gosse).The individual length of the eels ranged from 23.9 to65 cm (mean: 43.2 12.2), and the weight ranged from22 to 607 g (mean: 180.1 163.8). The eels were trans-ported to the laboratory in cool boxes and then dissectedto remove their organs. The muscle tissues of the eels werelyophilised and homogenised before analysis. A sample of0.1 g of the lyophilised muscle tissue was digested with4 ml of 25% tetra methyl ammonium hydroxide (TMAH)by using a microwave assisted extraction at 70 C for4 min. Then, 0.4 mL of the extract was adjusted to pH 4with an acetic acid/sodium acetate buer solution. Mercuryspecies were derivatised using NaBPr4 after the addition ofethyl mercury as an internal standard and after 5 min ofmechanical shaking they were extracted into isooctane forGCICP-MS (gas chromatographyinductively coupledplasma mass spectrometry) or GCMIP-AED (gas chro-matographymicrowave induced plasma atomic-emissiondetection) analysis. The analytical methodology has beenoptimised (see previous publications; Tseng et al., 1997;Moreno et al., 2006) and was validated by the analysis ofthe certied reference material DORM 2 (dogsh muscletissue from the National Research Council of Canada).The results obtained in the validation of the methodologywere in agreement using both detection techniques andare shown in Table 1.</p><p>The concentrations of the mercury species in muscle tis-sues of A. anguilla collected from the two sampling sites aresummarized in Table 2. The average concentration of totalHg was found to be 0.31 0.10 and 0.18 0.04 lg Hg g1</p><p>(expressed as wet weight) for the estuary and the ood-plains, respectively. These concentrations were always</p><p>below 0.5 lg Hg g1, which is the maximum set by theEuropean Union for total Hg in foodstus (CommissionRegulation No. 78/2005) and the admitted value set bythe World Health Organisation for human consumption(International Programme on Chemical Safety, Environ-mental Health Criteria No. 1, Mercury).</p><p>Higher MeHg values were encountered in the down-stream estuary (mean: 0.27 0.09 lg Hg g1 wet weight)compared to the oodplains, which averaged 0.11 0.03 lg Hg g1. As a result, most of the total mercury foundin the samples is present as MeHg (Table 2). Indeed, theaverage percentage of MeHg from the total mercury burdenwas found to be 86% in the samples from the estuary and65% in those from the oodplains. These numbers indicatethe need for applying specic speciation protocols to inves-tigate the environmental and toxicological impact of metal-lic contaminants.</p><p>Table 3 compares the results obtained in this work withthose collected from previous publications reporting totalmercury and MeHg levels in eels from dierent parts ofthe world. The results obtained for total mercury in theRiver Adour are of the same order of magnitude as otherpublished studies. However, MeHg can be only comparedwith a single study reporting MeHg concentrations in eelsfrom New Zealand (A. dieenbachii). Similar values areobtained in both studies in terms of concentration and per-centage of MeHg in the samples.</p><p>In contrast to the values from the estuary, MeHg con-centrations in the muscle tissues from the oodplains didnot change drastically in relation to the individual lengthsof the eels but nonetheless showed a signicant correlation(Fig. 2). Within the scatter observed for estuarine MeHgvalues, some eels showed MeHg concentrations close tothose found in the oodplains. This may be the conse-quence of eel life history, as they are able to migrate fromestuaries to either river or coastal habitats. Indeed, in arecent study in the Gironde estuary, Fablet et al. (2007)have shown, according to Sr:Ca proles in otoliths, that72% of the eels sampled changed their habitats once ormore. Thus, we cannot exclude the possibility that someof eels caught in the Adour estuary had recently come fromthe adjacent coastal or oodplain areas. Alternatively, thelarge spatial variability in the MeHg content in both sedi-ment and benthic food may also explain these results.</p><p>If the percentages of methyl mercury (normalised to thetotal mercury content) are considered, there is a clear linearregression between the length of the eels and MeHg relativeconcentrations, whatever the origin of eels (p value </p></li><li><p>Fig. 3). The correlation was higher in the oodplains. It isworth noticing that the lower MeHg concentrationsobtained for small eels in the oodplains indicates a lowerinitial exposure to MeHg. The higher slope indicates ahigher biomagnication rate versus the length of the shthan that obtained in the downstream estuary. Neverthe-less, both ecosystems show the same overall biomagnica-tion factor in the largest eels. These results can beexplained with regard to the dierent physical characteris-tics of both environmental compartments (i.e. salinity, foodavailability) and/or individual physiological characteristicssuch as growth rate.</p><p>Although there are still no data regarding contamina-tion levels and the reactivity of Hg in the Barthes, previ-</p><p>ous work in the Adour estuary has shown that mercuryspecies (particularly MeHg) were encountered in urban-related euents at signicantly higher levels compared tothe rivers draining upstream watersheds (Point, 2004).Moreover, Stoichev et al. (2006) reported that MeHg levelsin surface waters from the Adour estuary were character-ised by longitudinal variations, with highest concentrations(in both dissolved and particulate fractions) occurringwithin the downstream, urban estuarine area. This hasbeen explained not only by the high methylation potentialof the sediments, but also by direct anthropogenic inputs ofMeHg from specic discharge points. Such methylationpotential has been found to be enhanced under anaerobicconditions in sediments from the Adour River (Rodriguez</p><p>y = 0.002x + 0.027R2 = 0.643</p><p>FloodplainsEstuary</p><p>Length (cm)</p><p>y = 0.002x + 0.027R2 = 0.643</p><p>0</p><p>0.1</p><p>0.2</p><p>0.3</p><p>0.4</p><p>0.5</p><p>0.6</p><p>0 10 20 30 40 50 60 70</p><p>FloodplainsEstuary</p><p>MeH</p><p>gC</p><p>once</p><p>ntra</p><p>tion </p><p>( g </p><p>Hg </p><p>g -1 )</p><p>Fig. 2. Concentration of MeHg (lg Hg g1 wet weight) according to the length of eels from the downstream urban estuary and from the oodplains of theAdour River.</p><p>Table 3Comparison of total mercury and methyl mercury concentrations in eels obtained in similar studies (lg Hg g1 wet weight)</p><p>Species Location Type Total Hg MeHg Sample Refs.</p><p>A. Anguilla Vaccares (France) Pond 0.22 (n = 15) Liver Batty et al. (1996)A. Anguilla Berre (France) Pond 0.23 (n = 15) Liver Batty et al. (1996)A. Anguilla East Anglia (UK) River estuary 0.26 (n = 51) Muscle Edwards (1997)A. Anguilla East Anglia (UK) River broadening 0.10 (n = 51) Muscle Edwards (1997)A. dieenbachii Leith (New Zealand) River 0.12 (n = 1) 0.08 (n = 27...</p></li></ul>

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