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

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Page 1: Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

Baseline

Edited by Bruce J. Richardson

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

Ina Arleny a,b, Helene Tabouret c, Pablo Rodriguez-Gonzalez a, Gilles Bareille a,Olivier F.X. Donard a, David Amouroux a,*

a Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, IPREM CNRS UMR 5254, Universite de Pau et des Pays de l’Adour,

Helioparc, F-64053 Pau, Franceb Provincial Health Laboratory of Central Kalimantan, JI Let. Jend. Soeprato No1 Palangka Raya 73112, Kalimantan Tengah, Indonesia

c IFREMER, Laboratoire des Ressources Halieutiques d’Aquitaine, Technopole Izarbel, 64210 Bidart, France

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) andfinally 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, different 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 (>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).

The environmental and toxicological impact of Hg bio-accumulation in fish is related to the methylation of inor-

ganic mercury to form the more toxic methylmercury(MeHg) species. Fish tend to concentrate MeHg in theirtissues by a factor of 105–107, 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 specific redox gradientsand bacterial activity (Gilmour and Henry, 1991). Accord-ingly, A. anguilla may be an effective biomagnificator 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).

The River Adour (located at the South West of France)has a length of 335 km, enters the Atlantic Ocean at 43�30 0

North latitude 1�32 0 West longitude and drains a largeagricultural area of 17,000 km2. The Adour estuary isaffected 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, fisheries or recreational boating (Brunet andAstin, 1999). In the upstream estuarine zone, the river pre-sents large, flat man-made modified floodplains (knownlocally as the ‘‘Barthes’’) that constitute an area of15 km2, lying up to 2 km on both sides of the river. The

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 ‘Baseline—The New Format and Content’ (Mar. Pollut. Bull. 42, 703–704).

* Corresponding author. Tel.: +33 559 407 756; fax: +33 509 407 781.E-mail address: [email protected] (D. Amouroux).

www.elsevier.com/locate/marpolbul

Marine Pollution Bulletin 54 (2007) 1031–1071

Page 2: Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

Barthes are flooded twice a year and play a significanthydraulic and hydrological role owing their high storagecapacity. Such capacity, together with the existence ofman-made dykes, affords flood protection to the regionand allows a significant 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 fishermen 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).

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 biomagnification 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 biomagnification) to the higher lev-els of the food web, including human beings. A. anguilla

has 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-fined eels Anguilladieffenbachii from New Zealand (Redmayne et al., 2000).

Therefore, this is the first 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 different aquatic ecosystems of the Adour estuary.

This study is part of a research program, ‘‘Groupementde Recherche Adour’’ (GDR Adour), involving several lab-oratories that investigate possible effects of contaminantson dynamic eel populations. During this program, the sam-pling strategy was defined by the LRHA (Laboratoire deRessources Halieutique d’Aquitaine) – IFREMER (Insti-tute Francais pour l’Exploration de la Mer) according to,first, various phases characterizing the annual biologicalcycle of A. anguilla (colonization–sedentarisation–down-stream migration) and second, the specific 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.

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 floodplains (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 influenceof 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

N

AtlanticOcean

Tarnos

Urt

Anglet

Bayonne

N

AtlanticOcean Saline zone

Nive River

Kp 135

Kp 110110Kp 110

120Kp

Adour River

Gaves RiversFluvial zone

ADOUR ESTUARY

AdourEstuary

43°32’N

43°30’N

43°28’N

1°30’W 1°15’W1°20’W 1°10’W1°25’W

Downstream estuarine samplingsite (Redon zone)

Floodplain sampling site (Saint-Laurent de Gosse)

Fig. 1. Location of sampling areas in the lower estuary and upper estuary floodplain (Adour River, France).

1032 Baseline / Marine Pollution Bulletin 54 (2007) 1031–1071

Page 3: Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

catchments. It is also linked to the estuary only by valves,permitting at some point the input of fluvial water.

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 buffer 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 forGC–ICP-MS (gas chromatography–inductively coupledplasma mass spectrometry) or GC–MIP-AED (gas chro-matography–microwave 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 certified reference material DORM 2 (dogfish 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.

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 g�1

(expressed as wet weight) for the estuary and the flood-plains, respectively. These concentrations were always

below 0.5 lg Hg g�1, which is the maximum set by theEuropean Union for total Hg in foodstuffs (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).

Higher MeHg values were encountered in the down-stream estuary (mean: 0.27 ± 0.09 lg Hg g�1 wet weight)compared to the floodplains, which averaged 0.11 ±0.03 lg Hg g�1. 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 floodplains. These numbers indicatethe need for applying specific speciation protocols to inves-tigate the environmental and toxicological impact of metal-lic contaminants.

Table 3 compares the results obtained in this work withthose collected from previous publications reporting totalmercury and MeHg levels in eels from different 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. dieffenbachii). Similar values areobtained in both studies in terms of concentration and per-centage of MeHg in the samples.

In contrast to the values from the estuary, MeHg con-centrations in the muscle tissues from the floodplains didnot change drastically in relation to the individual lengthsof the eels but nonetheless showed a significant correlation(Fig. 2). Within the scatter observed for estuarine MeHgvalues, some eels showed MeHg concentrations close tothose found in the floodplains. 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 profiles 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 floodplain areas. Alternatively, thelarge spatial variability in the MeHg content in both sedi-ment and benthic food may also explain these results.

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 <0.01,

Table 1Results obtained for the analysis of certified reference material DORM 2(dogfish mussel tissue)

Analytical technique Concentrations in ng Hg g�1 (dry weight)

MeHg Hg(II) HgT

GC–ICP-MS 4319 ± 87 70 ± 18 4389 ± 92GC–MIP-AES 4096 ± 402 Not determined Not determinedCertified values 4470 ± 320 Not certified 4640 ± 260

Uncertainty of the results is expressed as 1s standard deviation.

Table 2Mean values of methyl mercury, inorganic mercury and total mercury concentrations (lg Hg g�1 wet weight) in the muscle tissues of A. anguilla collectedfrom the two sampling sites of the Adour estuary (uncertainty of the values is expressed as 1s standard deviation)

Sites n MeHg (lg Hg g�1) Hg(II) (lg Hg g�1) HgT (lg Hg g�1)

Mean ± SD Range Mean ± SD Range Mean ± SD Range

Estuary 15 0.27 ± 0.09 0.12–0.45 0.04 ± 0.03 0.003–0.13 0.31 ± 0.10 0.16–0.48Floodplains 7 0.11 ± 0.03 0.08–0.16 0.07 ± 0.05 0.004–0.16 0.18 ± 0.04 0.12–0.24

Baseline / Marine Pollution Bulletin 54 (2007) 1031–1071 1033

Page 4: Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

Fig. 3). The correlation was higher in the floodplains. It isworth noticing that the lower MeHg concentrationsobtained for small eels in the floodplains indicates a lowerinitial exposure to MeHg. The higher slope indicates ahigher biomagnification rate versus the length of the fishthan that obtained in the downstream estuary. Neverthe-less, both ecosystems show the same overall biomagnifica-tion factor in the largest eels. These results can beexplained with regard to the different physical characteris-tics of both environmental compartments (i.e. salinity, foodavailability) and/or individual physiological characteristicssuch as growth rate.

Although there are still no data regarding contamina-tion levels and the reactivity of Hg in the ‘‘Barthes’’, previ-

ous work in the Adour estuary has shown that mercuryspecies (particularly MeHg) were encountered in urban-related effluents at significantly 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 specific discharge points. Such methylationpotential has been found to be enhanced under anaerobicconditions in sediments from the Adour River (Rodriguez

y = 0.002x + 0.027R2 = 0.643

FloodplainsEstuary

Length (cm)

y = 0.002x + 0.027R2 = 0.643

0

0.1

0.2

0.3

0.4

0.5

0.6

0 10 20 30 40 50 60 70

FloodplainsEstuary

MeH

gC

once

ntra

tion

( µg

Hg

g -1)

Fig. 2. Concentration of MeHg (lg Hg g�1 wet weight) according to the length of eels from the downstream urban estuary and from the floodplains of theAdour River.

Table 3Comparison of total mercury and methyl mercury concentrations in eels obtained in similar studies (lg Hg g�1 wet weight)

Species Location Type Total Hg MeHg Sample Refs.

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. dieffenbachii Leith (New Zealand) River 0.12 (n = 1) 0.08 (n = 27) Muscle Redmayne et al. (2000)A. dieffenbachii Flemming (New Zealand) River 0.31 (n = 1) 0.48 (n = 34) Muscle Redmayne et al. (2000)A. dieffenbachii Kyeburne (New Zealand) River 0.65 (n = 1) 0.50 (n = 23) Muscle Redmayne et al. (2000)A. rostrata Savannah River (USA) River 0.15 (n = 24) Muscle Burger et al. (2001)A. Anguilla Thames River (UK) River 0.15 (n = 2) Muscle Yamaguchi et al. (2003)A. Anguilla La Capeliere (France) Pond 0.03 (n = 9) Muscle Ribeiro et al. (2005)A. Anguilla La Capeliere (France) Pond 0.06 (n = 10) Liver Ribeiro et al. (2005)A. Anguilla Fumemorte (France) Pond 0.09 (n = 9) Muscle Ribeiro et al. (2005)A. Anguilla Fumemorte (France) Pond 0.08 (n = 9) Liver Ribeiro et al. (2005)A. Anguilla Mornese (France) Pond 0.12 (n = 8) Muscle Ribeiro et al. (2005)A. Anguilla Mornese (France) Pond 0.15 (n = 8) Liver Ribeiro et al. (2005)A. Anguilla Yser (Belgium) River 0.15 (n = 8) Muscle Maes et al. (2005)A. Anguilla Meuse (Belgium) River 0.17 (n = 20) Muscle Maes et al. (2005)A. Anguilla Scheldt (Belgium) River 0.09 (n = 33) Muscle Maes et al. (2005)A. Anguilla Tiber River (Italy) River 0.23 (n = 8) Muscle Mancini et al. (2005)A. Anguilla Lesina (Italy) Lagoon 0.18 (n = 2) Muscle Storelli et al. (2007)A. Anguilla Adour River (France) River estuary 0.31 (n = 15 0.27 (n = 15) Muscle This workA. Anguilla Adour River(France) River floodplain 0.18 (n = 7) 0.11 (n = 7) Muscle This work

1034 Baseline / Marine Pollution Bulletin 54 (2007) 1031–1071

Page 5: Methylmercury bioconcentration in muscle tissue of the European eel (Anguilla anguilla) from the Adour estuary (Bay of Biscay, France)

Martin-Doimeadios et al., 2004). On the other hand, mer-cury species concentrations in coastal sediments from theAdour were found to be high enough to assess the impactof estuarine inputs on the nearby coastal area (Stoichevet al., 2004). Finally, in agreement with these results, MeHganalysis in three different trophic groups (suspension feed-ers, predators and deposit feeders) from different samplingsites of the downstream Adour estuary showed that MeHgis also subject to biomagnification in the benthic foodchains (Monperrus et al., 2005).

Taking into account these results, the high correlationsobtained for eels from the floodplains in (Figs. 2 and 3)can be explained by the population type and the exposuremode. Concerning the eels from the ‘‘Barthes’’, which is arelatively closed ecosystem, it can be assumed that expo-sure is mostly based on identical trophic routes providedby specific local food chains. On the other hand, becausethe downstream estuary receives an additional MeHg con-tribution from anthropogenic sources, various mercuryaccumulation routes related to different trophic chainscan be assumed.

Our research suggests a basis for large scale of studies inthe Adour estuary and provides, for the first time, prelimin-ary data on MeHg burdens, variability and compositionof mercury species in muscle tissues of European eels(A. Anguilla). In addition A. anguilla appears to be an effec-tive bioaccumulator of MeHg, even in aquatic environmentsmoderately contaminated by mercury, demonstrating theusefulness of this species as a bioindicator of the impactsof mercury pollution in different aquatic ecosystems.

Acknowledgements

This work is a contribution to the ‘‘Groupement deRecherche Adour’’ sponsored by the IFREMER, the Uni-versity de Pau et des Pays de l’Adour and the CNRS.I. Arleny acknowledges the French Ministry of ForeignAffair for her fellowship, H. Tabouret acknowledges

IFREMER and the Aquitaine Region for her Ph.D. grantand P. Rodriguez-Gonzalez acknowledges the ‘‘Secretariade Estado de Universidades e Investigacion’’ of the SpanishMinistry of Education and Science for his postdoctoral re-search fellowship. The authors are also grateful to N. Caill-Milly and P. Prouzet (LHA, IFREMER), the ConseilSuperieur de la Peche and MIGRADOUR for their helpin the field logistic and fish sampling.

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y = 1.82x - 7.35R2 = 0.93

y = 0.65x + 56.43R2 = 0.57

0 10 20 30 40 50 60 70Length (cm)

FloodplainsEstuary

p<0.01

p<0.01

-R2

R2

MeH

g (%

)

FloodplainsEstuary

p<0.01

p<0.01

y = 1.82x - 7.35R2 = 0.93

y = 0.65x + 56.43R2 = 0.57

FloodplainsEstuary

p<0.01

p<0.01

-R2

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50

60

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0025-326X/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.marpolbul.2007.04.004

Endocrine-disrupting phenols in selected riversand bays in the Philippines

Evangeline C. Santiago *, Charita S. Kwan

Research and Analytical Services Laboratory, Natural Sciences Research Institute, University of the Philippines,

Diliman, 1101 Quezon City, Philippines

Endocrine-disrupting (ED) compounds are known tointerfere with hormonal systems, affecting growth, develop-ment and reproduction in humans and animals (Colburnet al., 1993; Colon et al., 2000; Guo et al., 2001; Kogevinas,2001). Alkylphenols and bisphenols are among the waste-water pollutants that have been found to have ED proper-ties (Soto et al., 1995; Bustos-Obregon, 2001; Foster et al.,2001). Industrial effluents from chemical plants and micro-

bial processing of phenol derivatives can contribute to theload of alkylphenols and chlorophenols in natural waters(Junglaus et al., 1978; Lopez-Avila and Hites, 1980).

The presence of ED phenols in water bodies may havean adverse impact on fish. Exposures of swordtail fish at100 ppb nonylphenol indicated reproductive damage andaffected its growth (Kwak et al., 2001). Nonylphenol wasalso found to induce complete feminization of the gonadin genetically controlled all-male amago salmon (Nakam-ura et al., 2002). Many Filipinos depend on fishing andaquaculture for livelihood; thus, it is important to know

* Corresponding author. Tel.: +63 2920 7731; fax: +63 2928 6868.E-mail address: [email protected] (E.C. Santiago).

1036 Baseline / Marine Pollution Bulletin 54 (2007) 1031–1071