heavy metals of inshore benthic invertebrates from the barents sea

The Science of the Total Environment 306(2003) 99–110

0048-9697/03/$ - see front matter� 2002 Elsevier Science B.V. All rights reserved.PII: S0048-9697Ž02.00487-4

Heavy metals of inshore Benthic invertebrates from the BarentsSea

G.-P. Zauke *, B. Clason , V.M. Savinov , T. Savinovaa, a b,c b,c

Carl von Ossietzky Universitat Oldenburg, ICBM, Postfach 2503, D-26111 Oldenburg, Germanya ¨Akvaplan-niva, Polar Environmental Centre, N-9296, Tromsø, Norwayb

Murmansk Marine Biological Institute Kola Science Centre, Russian Academy of Sciences, 17, Vladimirskaya St., 19_83010,c

Murmansk, Russia

Received 12 April 2002; accepted 27 September 2002

Abstract

To assess metals in biota of the Barents Sea, information is presented on concentrations of Cu, Cd, Ni, Pb and Znin the marine inshore benthic invertebratesGammarus oceanicus, Littorina rudis, Nucella lapillus, Mytilus edulis andArenicola marina collected in summer 1994. For geographical comparisons, the metal content to body size relationshipwas taken into account due to the different body sizes found at the localities investigated. In general, our data providefurther evidence for the cadmium anomaly in invertebrates from polar waters which has been frequently discussed inthe literature, with Cd concentrations reaching 1 mg kg dry wt inG. oceanicus, 7 mg kg inL. rudis and 24 mgy1 y1

kg in N. lapillus. In contrast, our results obtained for Cd inM. edulis and A. marina are largely within a world-y1

wide reported range(1–2 and 0.2–0.9 mg kg , respectively). Although some severe Ni emissions in the Kola regiony1

(Russia) mainly from nickel smelters have been reported, we do not find indications of an enhanced Ni availabilityin the marine biota studied compared to other areas� 2002 Elsevier Science B.V. All rights reserved.

Keywords: Barents Sea; Biomonitoring; Cadmium-anomaly; Invertebrates; Metals

1. Introduction

Contamination of the Arctic marine ecosystemswith trace metals and other xenobiotics receivescontinued attention in the scientific literature andinternational environmental programmes(AMAP,1998; Dietz et al., 2000, 1996; Fant et al., 2001;Larsen et al., 2001; MacDonald and Bewers,

*Corresponding author. Tel.:q1615-327-7049; fax:q49-441-798-3701.

E-mail address: [email protected](G.-P.-P. Zauke).

1996). Predominant inputs of pollutants to theArctic occur by long-range transport, via oceanicwater mass exchanges and atmospheric processes,or are derived from local river discharges, run-offfrom land and industrial emissions(Alexander,1995; MacDonald et al., 2000; Pacyna, 1995;Pfirman et al., 1995). Recent estimates indicatethat approximately 52% of the general pollutionof the White Sea and the East Siberian Seas and75–80% of the pollution of the Barents, Kara andLaptev Sea are provided by the great Siberianrivers, mainly by the Rivers Ob and Yenisey

100 G.-P.-P. Zauke et al. / The Science of the Total Environment 306 (2003) 99–110

Fig. 1. Sampling locations for marine invertebrates in Russia(b: site 1 and 2) and Norway(a: site 3). Note that the co-ordinatesin (b) refer to the village of Dalniye Zelentsy(shaded area); the samplings sites 1 and 2 are only 0.5–1.0 km apart, a distance tooshort to be distinguished within the chosen grain of the co-ordinates.

(PAME, 1996). In addition, mining, metallurgicalindustries, offshore oil and gas exploration—whichare economically important for some Arctic coun-tries—as well as military activities, substantiallyincrease the contamination of the Barents Sea andthe Arctic Ocean(AMAP, 1998). In the Kolaregion, for example, mining and ore processingaccount for almost half of the industrial emission(Hansen et al., 1996) and are regarded as the mainanthropogenic source of trace metals in this area.Emissions from these industries mainly includecopper and nickel, but also aluminium, cadmium,iron, titanium, vanadium, chromium and zinc(Stanner and Bordeau, 1995).

Benthic invertebrates have been successfullyemployed in numerous biomonitoring studies

regarding, for example: amphipods(Clason andZauke, 2000; Zauke et al., 1995b); gastropods(DeWolf et al., 2000; Kang et al., 2000; Marigomezet al., 1998; Wright and Mason, 1999); bivalvia(Chase et al., 2001; Domouhtsidou and Dimitriad-is, 2000; Gutierrez-Galindo and Munoz-Barbosa,2001; Lionetto et al., 2001); and polychaetes(Wright, 1995; Wright and Mason, 1999). Beforesuch organisms can be used for this purpose thekinetics of metal uptake and depuration has to beevaluated. For the groups of organisms used inthis study, this has been done, clearly showingtheir suitability for biomonitoring(e.g. Bernds etal., 1998; Borgmann and Norwood, 1995; Clasonand Zauke, 2000; Fisher et al., 1996; Lares andOrians, 2001; Reinfelder et al., 1997; Ritterhoff et

101G.-P.-P. Zauke et al. / The Science of the Total Environment 306 (2003) 99–110

Table 1Quality assurance using certified reference materials randomlyallocated within the determinations

NIST SRM 1566 CRM 278(oyster tissue) (mussel tissue)

Analysed N Certified Analysed N Certified

Cu 70.0"6.4 19 63.0"3.5 9.2"0.9 19 9.6"0.16Cd 3.1"0.1 27 3.5"0.4 0.34"0.04 27 0.34"0.02Ni 1.1"0.1 15 1.03"0.19 1.1"0.2 16 (1.0)Pb 0.6"0.1 12 0.48"0.04 2.1"0.3 13 1.91"0.04Zn 827"78 15 852"14 74"2 16 76"2

Values are means"95% confidence intervals(mg kg dryy1

wt.). Limit of detection: 4.7(Cu); 0.23 (Cd); 0.5–1.0(Ni);0.5 (Pb); and 10(Zn) mg kg dry wt.(calculated after Butt-y1 ¨ner et al., 1980).

al., 1996; Wang et al., 1995). Generally, manyinshore benthic invertebrates have the advantageof being abundant, play an important role in theinshore foodweb and are easy to collect. Since, infield samples, organisms of different length occur,the possibility of a metal content to body sizerelationship has to be taken into account(e.g. Kimet al., 2001; Leung and Furness, 1999, 2001;Moore et al., 1991; Rainbow and Moore, 1986,1990; Tewari et al., 2000).

Among inshore benthic invertebrates, differentfeeding strategies and life histories can be found.Gammaridean amphipods are mainly omnivorous(e.g. Macneil et al., 1997; Rinderhagen et al.,2000) and reproduce without meroplanktic larvae,whereas gastropods and bivalvia reproduce withsuch larvae. Their feeding strategy vary fromherbivorous(Littorina) and carnivorous(Nucella)to filter feeding(Mytilus) (e.g. Carroll and Highs-mith, 1996; Cranford and Hill, 1999; Jorgensen,1996; Kim and DeWreede, 1996; Penney et al.,2001). Analysing such a broad ecological range oforganisms seems to be more adequate to assessthe environmental quality than a single speciesstudy, because different paths of metal uptake areimplicitly taken into account.

The utilisation of invertebrates for biomonitor-ing of metals in Arctic waters is part of the AMAPapproach. However, while substantial informationis available for some parts of the Arctic, especiallyGreenland and Canada(see literature compilationin AMAP 1998), there is a data gap for benthicinshore invertebrates from the Barents Sea region.In this paper, we provide such information on themetals Cu, Cd, Ni, Pb and Zn in selected amphi-pods, gastropods, bivalvia and polychaetes.

2. Materials and methods

2.1. Sampling and sample preparation

The invertebrate samples were collected in July1994 at three localities at the Barents Sea, twosites in Russia(Dalniye Zelentsy, Fig. 1b; site 1and 2) and one site in Norway(Hornoya, Fig. 1a,site 3). We considered the following species for ageographical comparison: the amphipodGamma-rus oceanicus Segerstrale, 1947(site 1–3) and the˚gastropodsLittorina rudis (Maton, 1797) (site 2

and 3) andNucella lapillus (Linnaeus, 1758) (site2 and 3). Other species were only found at onesite and are included in this study for a broadertaxonomic range: the bivalveMytilus edulisLineaeus, 1758(site 2); and the polychaeteAren-icola marina Lineaeus, 1758(site 1). The animalswere collected at low tide from rocky shores andwere kept for 24 h in aerated seawater for defe-cation, with the only exception ofA. marina whichwas sampled from a sandy tide flat and was keptalive under wet filter paper. Subsequently, theorganisms were frozen aty27 8C in polypropyleneand polystyrene containers and transferred on dryice to the University of Oldenburg for furtheranalyses. Replication was achieved at the level ofindividual organisms which were independentlyprocessed and analysed to allow the assessment ofthe possible size dependency of metal accumula-tion. The body length of gammarids were assayedwith scaled paper according to Meurs and Zauke(1988); for the gastropods and bivalvia the shelllength was evaluated with the aid of an electroniccalliper rule.

2.2. Analytical procedures

Upon arrival at the laboratory, the samples wereseparated and further processed as biological spec-imen, viz. lyophilised(using the instrument AlphaI, manufactured by Christ Gefriertrocknungsanla-gen GmbH, Osterode am Harz, Germany) andsubsequently homogenised using a boron carbidemortar and pestle. Aliquots of approximately 10


Table 2Comparison of mean metal concentrations(mg kg dry wt.) in Gammarus oceanicus from different sites of the Barents Seay1

(summer 1994)

Variable Site N Mean"95%CI Test Groups Linear regression:

1 2 3variable vs. body length

Const Slope Adj.R2

Body length 1 60 19.8"0.8 NK ± – – –2 60 20.8"1.0 ± – – –3 20 23.3"2.1 ± – – –

Cu 3 20 14"2 NK ± 20 y0.26 0.0501 57 20"2 ± 28 y0.36 0.0132 55 28"3 ± 35 y0.35 0.003

Cd 1 59 0.67"0.12 Z ± 1.00 y0.02 0.0002 58 0.85"0.14 ± 0.89 y0.00 0.0003 20 1.01"0.33 ± y0.10 0.05 0.047

Ni 1 52 1.3"0.2 NK ± 2.0 y0.04 0.0222 53 1.5"0.2 ± 1.3 0.01 0.0003 17 2.4"0.4 ± 4.8 y0.10 0.357

Pb 2 44 -0.5 N.a. – – –3 17 -0.5 – – –1 42 -0.5 – – –

Zn 1 58 61"3 Z ± 64 y0.18 0.0002 59 65"3 ± ± 64 0.03 0.0003 20 68"4 ± 48 0.84 0.187

N LIP LS (P) Test Stat(P)L 140 0.015 2.79(0.065) F 6.69(0.002)Cu 132 0.346 7.03(0.001) W 46.2 (0.000)Cd 137 0.000 N.a. H 6.71(0.035)Ni 122 0.013 1.47(0.234) F 19.2(0.000)Pb 103 N.a. N.a. N.a. N.a.Zn 137 0.004 N.a. H 12.2(0.002)

Means which do not differ significantly are joined to groups by vertical bars(±).Tests of normality(LIP) and of equality ofvariances(LS) and means(Test; Stat). Site: see Fig. 1(note that the sequence follows increasing means and might differ betweenvariables); Test (multiple comparison tests): NKsStudent–Newman–Keuls Multiple Range Test; ZsZ-statistic; Varsvariable;N:individual organisms analysed(note thatN might differ between variables due to possible failures in the multi-element determinationof the unique samples); CIsconfidence intervals; n.a.snot applicable; LIPsLilliefors probabilities(2-tail); LSsLevene statistic;FsF statistic(classical ANOVA); WsWelch statistic; HsKruskal–Wallis test statistic;Pstail probability.

mg dried material were digested for 1 h at 968Cwith 50 ml HNO (70–71%, Baker Instra-Ana-3

lysed) in 1.5 ml Eppendorf reaction tubes(safelock). After appropriate dilution, the final sampleand standard solutions were adjusted to concentra-tions of 1.75% HNO and 2% Triton X-100. The3

elements Cd, Pb, Ni and Cu were assayed usingsequential multi-element graphite tube atomicabsorption spectroscopy (Varian Techtron,SpectrAA-30, GTA-96, wall atomisation) and Zee-man background correction(wavelengths: 228.8,217.0, 232.0 and 324.8 nm; atomisation tempera-tures: 2300, 2400, 2700 and 25008C, respective-

ly). For Cd and Pb, a palladium nitrate matrixmodifier was employed(10.0"0.2 g l in 15%y1

HNO ). Zn was measured in an air-acetylene flame3

(SpectrAA-300, deuterium background correction;wavelength 213.9 nm) using a manual micro-injection method(100-ml sample volume). Qualityassurance followed German GLP regulations. Pre-cision and validity were assessed with the aid ofcertified reference materials which were randomlyallocated within the determinations(Table 1). Lim-its of detection were calculated as 2.6 standarddeviations from measurements of a ‘low sample’with blanks set to zero(Buttner et al., 1980),¨


Table 3Comparison of mean metal concentrations(mg kg dry wt.) in Littorina rudis from different sites of the Barents Sea(summery1

1994)


1 2variable vs. shell length

Const Slope Adj.R2

Shell length 2 20 14.2"0.9 NK ± – – –3 20 16.0"0.9 ± – – –

Cu 3 20 32"8 NK ± 21 0.72 0.0002 19 39"8 ± y30 4.91 0.225

Cd 2 20 2.5"1.2 Z ± 13 y0.75 0.2643 20 7.1"2.8 ± 28 y1.32 0.135

Ni 2 17 3.2"0.8 NK ± 3.7 y0.04 0.0003 18 4.8"1.0 ± y0.7 0.34 0.059

Pb 2 17 0.66"0.12 NK ± 1.3 y0.04 0.0653 17 0.68"0.14 ± 1.8 y0.07 0.246

Zn 2 20 75"6 NK ± 52 1.63 0.0003 20 85"8 ± 104 y1.22 0.000

N LIP LS (P) Test Stat(P)L 40 0.533 0.00(0.959) p-T y3.02 (0.005)Cu 39 0.189 0.33(0.570) p-T 1.23(0.226)Cd 40 0.000 N.a. M-W 55.0(0.000)Ni 35 0.189 1.56(0.221) p-T y2.67 (0.012)Pb 34 0.410 0.10(0.754) p-T y0.26 (0.798)Zn 40 0.115 0.37(0.546) p-T y1.98 (0.055)

Tests of normality(LIP) and of equality of variances(LS) and means(Test; Stat) Means which do not differ significantly arejoined to groups by vertical bars(±). p-Tspooled variancet-test; M–WsMann–Whitney test(note thatN might differ betweenvariables due to possible failures in the multi-element determination of the unique samples); otherwise as in Table 2.

preferably using reference materials. All metalconcentrations in animal tissues are reported in mgkg (mg g ) dry weight (dry wt.). Water con-y1 y1

tents are: 65.5% forG. oceanicus; 72.0% for L.rudis; 72.2% forN. lapillus; 83.6% forM. edulis;and 80.3% forA. marina, leading wet wt.ydry wt.ratios of 2.9, 3.6, 3.6, 4.0, 6.4 and 5.0, respectively.

2.3. Statistical procedures

As mentioned above, replication was achievedat the level of individual organisms which wereindependently processed and analysed. Thehypothesis of normal distribution was tested usingthe Lilliefors test provided in SYSTAT for Win-dows, Version 8.0(Wilkinson, 1998, p. 711).Further statistical evaluation was performed usingBMDP Dynamics, either non-parametric statisticsor one- and two-way analysis of variance withdata screening(Dixon, 1992), depending on the

results of the Lilliefors test. First, global nullhypotheses(equality of means between the sitesinvestigated) were tested either by Kruskal–Wallistest, classical ANOVA(assuming equality of var-iances) or by non-classical Welch Test(not assum-ing equality of variances). The adequate procedurewas selected after testing equality of variances byLevene Test. Null hypotheses were rejected at 95%significance level(P-0.05). Second, heterogene-ity was analysed in more detail using the multiplecomparison option(ZSTAT) or the Student–New-man–Keuls Multiple Range Test(NK) (as0.05).The robust NK procedure involves an adjustedsignificance level for each group of ordered means(Dixon, 1992; p. 585). BMDP outputs do notinclude values for the test statistic but only providegraphical information(that is, means which do notdiffer significantly are joined to groups by verticalbars). The advantage of this procedure is thatresults are readily available(see Tables 2–4), in


Table 5Metal concentrations(mg kg dry wt.) of inshore inverte-y1

brates from the Barents Sea(summer 1994)

Species Variable Site N Mean"95%CI LIP

M.e. Shell length 2 20 30.0"1.9 0.653M.e. Cu 2 20 8.9"1.2 0.678M.e. Cd 2 20 2.0"0.2 1.000M.e. Ni 2 20 2.9"0.4 0.508M.e. Pb 2 16 1.6"0.3 0.001M.e. Zn 2 20 89"15 0.000A.m. Cu 1 10 6.8"1.8 1.000A.m. Cd 1 10 0.34"0.27 0.002A.m. Ni 1 10 11"3 0.360A.m. Pb 1 10 0.8"0.3 0.135A.m. Zn 1 10 47"12 0.292

M.e.: Mytilus edulis; A.m: Arenicola marina (note thatNmight differ between variables due to possible failures in themulti-element determination of the unique samples); otherwiseas in Table 2.

Table 4Comparison of mean metal concentrations(mg kg dry wt.) in Nucella lapillus from different sites of the Barents Sea(summery1

1994


1 2variable vs. shell length

Const Slope Adj.R2

Shell length 2 20 22.4"1.8 NK ± – – –3 20 25.6"2.4 ± – – –

Cu 3 20 46"11 NK ± 81 y1.36 0.0462 19 66"17 ± 93 y1.22 0.000

Cd 3 20 16"5 NK ± y1.8 0.68 0.0472 20 24"5 ± 12.5 0.53 0.000

Ni 3 17 1.9"0.3 NK ± 0.8 0.04 0.0292 18 2.3"0.4 ± 0.0 0.11 0.219

Pb 2 18 0.9"0.2 NK ± 0.3 0.03 0.0173 17 1.9"0.3 ± 0.8 0.04 0.019

Zn 3 20 416"125 NK ± 152 10.32 0.0002 20 553"129 ± 510 1.92 0.000

N LIP LS (P) Test Stat(P)L 40 0.326 1.71(0.199) p-T y2.23 (0.032)Cu 40 0.250 3.54(0.067) p-T 2.09(0.044)Cd 39 0.021 0.09(0.768) p-T 2.48(0.018)Ni 35 0.151 0.53(0.473) p-T 1.91(0.064)Pb 35 0.036 8.36(0.007) s-T y5.14 (0.000)Zn 40 0.052 0.75(0.391) p-T 1.61(0.117)

Tests of normality(LIP) and of equality of variances(LS) and means(Test; Stat). s-Tsseparate variancet-test (note thatNmight differ between variables due to possible failures in the multi-element determination of the unique samples); otherwise as inTable 2.). Means which do not differ significantly are joined to groups by vertical bars(±).

contrast, for example, to outputs of pairwiset-tests(adjusted to multiple comparisons) which wouldhave been adequate too. Possible metal content tobody size relationships were evaluated using linearregression analysis(Wilkinson, 1998). The signif-icance was assessed by inspection of adjustedR -2

values.

3. Results

The results of the QA procedure are summarisedin Table 1. The analysed values for the referencematerials are largely in good agreement with thecertified values and the limits of detection aresufficiently low for the purpose of this study, withthe only exception of Pb where gammarids provedto be below this value.

Results of the metal determinations of inshoreinvertebrates are compiled in Tables 2–5. Accord-ing to results of the Lilliefors test(LIP), the


hypothesis of normality has to be rejected(as0.01) in a few cases only(Cd and Zn in G.oceanicus; Cd in L. rudis; Pb in M. edulis; andCd in A. marina). Regarding the multiple compar-ison tests, a distinct heterogeneity between sam-pling sites can be observed in many cases, e.g. forCu and Ni inG. oceanicus (Table 2), Cd and Niin L. rudis (Table 3) and Cu, Cd and Pb inN.lapillus (Table 4). Furthermore, some metals showa distinct variation with respect to the speciesinvestigated, with highest Cu, Cd and Zn concen-trations inN. lapillus.

Results of the linear regression analyses supporthypotheses of clear relationships between metalconcentrations and body or shell length of individ-ual organisms only in a few cases: viz. Ni and Znin G. oceanicus (Table 2; R s0.357, Ps0.0072

and R s0.187,Ps0.033) as well as Cu, Cd and2

Pb in L. rudis (Table 3; R s0.225, Ps0.023;2

R s0.264, Ps0.012 andR s0.246, Ps0.025,2 2

respectively). A significant R -value for Ni in N.2

lapillus (Table 4;R s0.219,Ps0.029) is largely2

due to one outlier and will not be considered. Inall other cases, failure to obtain significant rela-tionships is mainly due to slopes not differingfrom zero andyor due to a large variability of theindividual metal concentrations but not to an inad-equate choice of the linear model.

4. Discussion

4.1. Interaction between size of organisms andgeographical heterogeneity

It appears from Tables 2–4, that for all threespecies investigated, significant differences in bodyor shell length are obtained between the Russiansites (1 andyor 2) and the Norwegian site(3),leading to the question whether significant differ-ences in metal concentrations in biota are due toa geographical heterogeneity or due to a sizedependency. In all cases where no significant linearregression between incorporated metals and lengthwas found, the answer is in favour of a geograph-ical heterogeneity. When a significant linear regres-sion was obtained for a specific site, the modelwas used to adjust the metal concentration to thelength of the other sites under consideration.

Regarding Ni inG. oceanicus from site 3 (Table2) the adjusted value for a length of 19.8 mmwould be 2.8 compared to the measured value of2.4 mg kg . We can thus infer that the detectedy1

significant differences are conservative and site-dependent. Regarding Zn we find two overlappinggroups. The corresponding adjusted Zn value forsite 3 would be 65 mg kg , suggesting no cleary1

differences between the sites. RegardingL. rudis(Table 3), adjusted Cu concentrations of site 2 toa length of 16.0 mm would be 49 compared to 39mg kg and adjusted Pb concentrations of site 3y1

to a length of 14.2 mm would be 0.81 comparedto 0.68 mg kg . In both cases, we did not findy1

significant differences but this may eventually bethe case taking the metal content to shell lengthdependency into account. The significant differ-ence found for Cd seems to be conservative as canbe inferred from an adjusted value of 1.0 comparedto 2.5 mg kg for site 2.y1

4.2. Comparison of metal levels between speciesof this study

Trace metal concentrations obtained in this studyand those reported for various marine invertebratesfrom different regions are compiled in Table 6.Comparing the metal levels between species ofthis study we find highest Cd concentrations inthe carnivorous gastropodN. lapillus, intermediateones in the herbivorous gastropodL. rudis and thefilter feeding musselM. edulis and lowest concen-trations in the omnivorous amphipodG. oceanicusand sediment feeding polychateA. marina. Thereare two possible reasons to explain this sequence.The first points to the different feeding strategiesof the organisms investigated. However, detailedinformation on the biomagnification processes forCd in these organisms is not available. Further-more, gastropods may accumulate more Cd due tothe relatively large portion of the midgut glandcompared to the other organisms which is animportant target for this element(Viarengo andNott, 1993). A similar sequence is found for theelements Cu and Zn.

4.3. Comparison of locations of this study

This comparison requires the consideration ofinteractions between size-dependent metal uptake


Table 6Metal concentrations in selected marine invertebrates reported in the literature(mg kg dry wt.)y1

Species Ref. Location Cu Cd Ni Pb Zn

Gammarus 1 Barents Sea(site 2) 28 0.9 1.5 -1 65oceanicus (site1) 20 0.7 1.3 -1 61

(site 3) 14 1.0 2.4 -1 68Gammarus salinus 2 Elbe-, Weser estuarya 86–135 0.3–0.5 – 1.6–2.8 73–91Gammarus salinus 3 Weser estuarya 75 0.4 – 1.3 62Gammarus locustra 4 German Bighta 64 0.12 – 2.0 51Gammarus setosus 5 Cape Hatt, Canada – 0.75 – – –Littorina rudis 1 Barents Sea(site 2) 39 2.5 3.2 -1 75

(site 3) 32 7.0 4.8 -1 85Littorina rudis 6 Avola estuaryb 333–695 0.9–1.8 – 28–44 193–552Littorina rudis 6 Avola estuaryc 130–207 0.7–1.6 – 12–48 242–279Littorina littorea 7 Estuaries(GB)d 417–692 2–13 5.5–6.9 4–11 141–345Littorina littorea 7 Estuaries(GB)e 135–137 1.6 1.5–2.8 1.9–2.0 77–80Littorina littorea 8 Estuaries(GB)f 44–87 0.6–0.7 5.6–9.1 0.5–0.9 52–80Littorina littorea 9 Shannon(Ireland) 23 – 72 – 66Littorina obtusata 9 Shannon(Ireland) 18 – 27 – 65Nucella lapillus 1 Barents Sea(site 2) 66 24 2.3 -1 553

(site 3) 46 16 1.9 1.9 416Nucella lapillus 9 Shannon(Ireland) 45 – 5.1 – 214Mytilus edulis 1 Barents Sea(site 2) 8.9 2.0 2.9 1.6 89Mytilus edulis 9 Shannon(Ireland) 7.0 – 3.0 – 88Mytilus edulis 8 Estuaries(GB)f 8–14 1.4–2.2 13–30 3.2–5.9 115–191Mytilus edulis 10 Norderneya 11–14 0.5–0.9 – 1.2–2.7 62–122Mytilus edulis 11 Godthaab Fjordg 8.6 1.8 – 1.7 93Mytilus edulis 12 Island 9.6 0.6 – 0.8 162Mytilus edulis 13 Chupa estuaryh 4.5–4.9 4.9–5.1 – 0.5–0.7 53–67Mytilus edulis 14 WMWi 7.9 2.0 2.2 5.0 130Arenicola marina 1 Barents Sea(site 1) 6.8 0.34 11 0.8 47Arenicola marina 8 Estuaries(GB)f 18–29 0.8–0.9 6–96 1.4–1.5 138–163Arenicola marina 10 Norderneya 10–30 0.4–0.9 – 1.5–2.0 81–91Arenicola marina 15 German Wadden Seaa 8–21 0.2–0.9 – 1.0–2.4 –

Ref: 1: This study; 2: Zauke et al.(1988); 3: Clason(1996); 4: Clason and Zauke(2000); 5: MacDonald(1988); 6: Wilson(1982); 7: Bryan and Gibbs(1983); 8: Wright and Mason(1999); 9: Oleary and Breen(1997); 10: Zauke et al.(1995a); 11: Rigetet al. (1996); 12: Olafsson(1986); 13: Millward et al.(1999); 14: Bernds et al.(1998); 15: Lorch et al.(1990).

North Sea.a

Ireland(upper reach of a pollution gradient).b

Ireland(lower reach of a pollution gradient).c

Contaminated sites(Fal, Thames).d

Uncontaminated sites(Teifi, Orwell).e

Eastern England(Orwell, Stour).f

Greenland.g

White Sea(Russia).h

World Mussel Watch Data Base(overall median value).i

and geographical heterogeneity as discussed above.In most cases, geographical differences foundbecome more obvious after consideration of size-dependent effects. However, there is no consistenttrend of metal concentrations in biota between theNorwegian and Russian sites. In summary, there

appears to be more Cu in biota from the Russiansite 2, but more Ni and(to some extent) Pb inbiota from the Norwegian site 3. No tendency isfound for Cd and Zn. Thus, we cannot infer ageneral increased bioavailability for heavy metalsin the organisms from any of the sites investigated.


4.4. Comparison of Arctic data to other regions

Regarding gammaridean amphipods, the datasuggest somewhat enhanced Cd concentrations inpolar samples, while corresponding copper concen-trations seem to be rather low. All other elementsare within the same range including uncontami-nated samples from temperate regions. Availabledata for gastropods of the genusLittorina point tosome severe contamination problems in Britishestuaries(see notes b–f in Table 6), especially forCu, Pb and Zn. Compared to data from uncontam-inated sites, metal concentrations inL. rudis arelower or within the same range, again with theonly exception of Cd. For the gastropodN. lapillusalmost no information is available in the literature.Available data for the musselMytilus edulis arerather homogeneous, not far apart from an overallmedian value reported in the world mussel watchdata base. Likewise, most of the reported metalconcentrations in lugworms(A. marina) are withinthe same range, with the only exception of someelevated levels in organisms from British estuaries.A comparison of metal concentrations in inverte-brates to those of higher order animals(fish,mammals, birds) is not advisable, since the firstrepresent whole body concentrations while thelatter are largely related to specific organs. If thisis intended, a complete mass balance of elementswould be required.

In general, our data onGammarus andLittorinaprovide to some extent further evidence for thecadmium anomaly in invertebrates from polarwaters which has been frequently discussed in theliterature(Bargagli et al., 1996; Bustamante et al.,1998; Demoreno et al., 1997; Petri and Zauke,1993; Ritterhoff and Zauke, 1997). Extreme highCd concentrations in Antarctic crustaceans, relatedto indications of a Cu deficiency, were inferred byPetri and Zauke(1993). It has been hypothesised,that a potential copper deficiency might be relatedto an increased uptake of Cd due to a insufficientselectivity of the uptake process for the essentialelement Cu.

A similar potential copper deficiency might bededuced from the relatively low values found inG. oceanicus and L. rudis from the Barents Sea.Although some severe Ni emissions in the Kola

region (Russia) mainly from nickel smelters havebeen reported(Chekushin et al., 1998; Gregureket al., 1998; Kelley et al., 1995; Lindroos et al.,1998), we do not find indications of an enhancedNi availability in the marine biota studied com-pared to other areas.

Acknowledgments

We thank Murmansk Marine Biological Institutefor invitation to Dalniye Zelentsy(Russia) and J.Ritterhoff for his help during the field work. Travelto Murmansk was funded by Kernforschungszen-trum Karlsruhe (Stabsabteilung InternationaleBeziehungen); we thank K. Wiendieck for his kindsupport. The assistance of A. Wicker and C.Pfeiffer in the analytical work is gratefullyacknowledged.

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