Heavy Metals of Inshore Benthic Invertebrates from the Barents

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					         Heavy Metals of Inshore Benthic Invertebrates from the Barents Sea*

                 G.-P. Zauke1, B. Clason 1 ,V.M. Savinov2,3 & T. Savinova2,3




    1
        Carl von Ossietzky Universität Oldenburg, ICBM, Postfach 2503, D-26111 Oldenburg, Germany
                 2
                   Akvaplan-niva, Polar Environmental Centre, , N-9296, Troms , Norway
                                                                                ǿ
        3
          Murmansk Marine Biological Institute Kola Science Centre, Russian Academy of Sciences, 17,
                              Vladimirskaya St., 19\83010, Murmansk, Russia




Abstract
To assess metals in biota of the Barents Sea, information is presented on concentrations of
Cu, Cd, Ni, Pb and Zn in the marine inshore benthic invertebrates Gammarus oceanicus, Lit-
torina rudis, Nucella lapillus, Mytilus edulis and Arenicola marina collected in summer 1994.
For geographical comparisons the metal content to body size relationship was taken into ac-
count due to the different body sizes found at the localities investigated. In general our data
provide further evidence for the cadmium anomaly in invertebrates from polar waters which
has been frequently discussed in the literature, with Cd concentrations reaching 1 mg kg-1 dry
wt in G. oceanicus, 7 mg kg-1 in L. rudis and 24 mg kg-1 in N. lapillus. In contrast, our results
obtained for Cd in M. edulis and A. marina are largely within a world-wide reported range (1-
2 and 0.2-0.9 mg kg-1, respectively). Although some severe Ni emissions in the Kola region
(Russia) mainly from nickel smelters have been reported, we do not find indications of an en-
hanced Ni availability in the marine biota studied compared to other areas



Keywords: Barents-Sea, biomonitoring, cadmium-anomaly, invertebrates, metals




*
    pre-print - The Science of the total Environment 306/1-3: 99 – 110 (2003)
                                              2

1. Introduction
Contamination of the Arctic marine ecosystems with trace metals and other xenobiotics re-
ceives continued attention in the scientific literature and international environmental pro-
grammes (AMAP 1998; Dietz et al. 2000; Dietz et al. 1996; Fant et al. 2001; Larsen et al.
2001; Macdonald and Bewers 1996). Predominant inputs of pollutants to the Arctic occur by
long-range transport, via oceanic water mass exchanges and atmospheric processes, or are de-
rived from local river discharges, run-off from land and industrial emissions (Alexander 1995;
MacDonald et al. 2000; Pacyna 1995; Pfirman et al. 1995). Recent estimates indicate that
about 52% of the general pollution of the White Sea and the East Siberian Seas and 75-80%
of the pollution of the Barents, Kara and Laptev Sea are provided by the great Siberian rivers,
mainly by the Rivers Ob and Yenisey (PAME 1996). In addition, mining , metallurgical in-
dustries, off-shore oil and gas exploration — which are economically important for some
Arctic countries — as well as military activities substantially increase the contamination of
the Barents Sea and the Arctic Ocean (AMAP 1998). In the Kola region, for example, mining
and ore processing account for almost half of the industrial emission (Hansen et al. 1996) and
are regarded as the main anthropogenic source of trace metals in this area. Immissions from
these industries mainly include copper and nickel, but also aluminium, cadmium, iron, tita-
nium, vanadium, chromium, and zinc (Stanner and Bordeau 1995).
Benthic invertebrates have been successfully employed in numerous biomonitoring studies,
regarding, for example, amphipods (Clason and Zauke 2000; Zauke et al. 1995b), gastropods
(De Wolf et al. 2000; Kang et al. 2000; Marigomez et al. 1998; Wright and Mason 1999), bi-
valvia (Chase et al. 2001; Domouhtsidou and Dimitriadis 2000; Gutierrez-Galindo and Mu-
noz-Barbosa 2001; Lionetto et al. 2001) and polychaetes (Wright 1995; Wright and Mason
1999). Before such organisms can be used for this purpose the kinetics of metal uptake and
depuration has to be evaluated. For the groups of organisms used in this study this has been
done, clearly showing their suitability for biomonitoring (e.g. Bernds et al. 1998; Borgmann
and Norwood 1995; Clason and Zauke 2000; Fisher et al. 1996; Lares and Orians 2001; Rein-
felder et al. 1997; Ritterhoff et al. 1996; Wang et al. 1995). Generally, many inshore benthic
invertebrates have the advantage of being abundant, play an important role in the inshore
foodweb and are easy to collect. Since in field samples organisms of different length occur,
the possibility of a metal content to body size relationship has to be taken into account (e.g.
Kim et al. 2001; Leung and Furness 1999; Leung and Furness 2001; Moore et al. 1991; Rain-
bow and Moore 1986; Rainbow and Moore 1990; Tewari et al. 2000).
Among inshore benthic invertebrates different feeding strategies and life histories can be
found. Gammaridean amphipods are mainly omnivorous (e.g. Macneil et al. 1997; Rinder-
hagen et al. 2000) and reproduce without meroplanktic larvae, whereas gastropods and bival-
via reproduce with such larvae. Their feeding strategy vary from herbivorous (Littorina) and
carnivorous (Nucella) to filter feeding (Mytilus) (e.g Carroll and Highsmith 1996; Cranford
and Hill 1999; Jorgensen 1996; Kim and DeWreede 1996; Penney et al. 2001). Analysing
such a broad ecological range of organisms seems to be more adequate to assess the environ-
mental quality than a single species study, because different paths of metal uptake are implic-
itly taken into account.
The utilisation of invertebrates for biomonitoring of metals in Arctic waters is part of the
AMAP approach. However, while substantial information is available for some parts of the
Arctic, especially Greenland and Canada (see literature compilation in AMAP 1998), there is
a data gap for benthic inshore invertebrates from the Barents Sea region. In this paper we pro-
vide such information on the metals Cu, Cd, Ni, Pb and Zn in selected amphipods, gastro-
pods, bivalvia and polychaetes.
                                               3

2. Materials and methods
2.1. Sampling and sample preparation
The invertebrate samples were collected in July 1994 at three localities at the Barents Sea,
two sites in Russia (Dalniye Zelentsy, Fig. 1B; site 1 and 2) and one site in Norway (Hornoya,
Fig. 1A, site 3). We considered the following species for a geographical comparison: the am-
phipod Gammarus oceanicus Segerstråle, 1947 (site 1-3) and the gastropods Littorina rudis
(Maton, 1797) (site 2 and 3) and Nucella lapillus (Linnaeus, 1758) (site 2 and 3). Other spe-
cies were only found at one site and are included in this study for a broader taxonomic range:
the bivalve Mytilus edulis Lineaeus, 1758 (site 2) and the polychaete Arenicola marina Lin-
eaeus, 1758 (site 1). The animals were collected at low tide from rocky shores and were kept
for 24h in aerated seawater for defecation, with the only exception of A. marina which was
sampled from a sandy tide flat and was kept alive under wet filter paper. Subsequently, the
organisms were frozen at –27° C in polypropylene and polystyrene containers and transferred
on dry ice to the University of Oldenburg for further analyses. Replication was achieved at the
level of individual organisms which were independently processed and analysed to allow the
assessment of the possible size dependency of metal accumulation. The body length of gam-
marids were assayed with scaled paper according to Meurs and Zauke (1988); for the gastro-
pods and bivalvia the shell length was evaluated with the aid of an electronic calliper rule.


2.2. Analytical Procedures
Upon arrival at the laboratory the samples were separated and further processed as biological
specimen, viz. lyophilised (using the instrument ALPHA I, manufactured by Christ Gefrier-
trocknungsanlagen GmbH, Osterode am Harz, Germany) and subsequently homogenised us-
ing a boron carbide mortar and pestle. Aliquots of about 10 mg dried material were digested
for 1 h at 96°C with 50 µl HNO3 (70-71%, Baker Instra-Analysed) in 1.5 ml Eppendorf reac-
tion tubes (safe lock). After appropriate dilution, the final sample and standard solutions were
adjusted to concentrations of 1.75 % HNO3 and 2 % Triton X-100. The elements Cd, Pb, Ni
and Cu were assayed using sequential multielement graphite tube atomic absorption spectros-
copy (Varian Techtron, SpectrAA-30, GTA-96, wall atomisation) and zeeman background
correction (wavelengths: 228.8, 217.0, 232.0 and 324.8 nm; atomisation temperatures: 2300,
2400, 2700 and 2500°C, respectively). For Cd and Pb, a palladium nitrate matrix modifier
was employed (10.0 ± 0.2 g l-1 in 15% HNO3). Zn was measured in an air-acetylene flame
(SpectrAA-300, deuterium background correction; wavelength 213.9 nm) using a manual mi-
cro-injection method (100 µl sample volume). Quality assurance followed German GLP
regulations. Precision and validity were assessed with the aid of certified reference materials
which were randomly allocated within the determinations (Table 1). Limits of detection were
calculated as 2.6 standard deviations from measurements of a "low sample" with blanks set to
zero (Büttner et al. 1980), preferably using reference materials. All metal concentrations in
animal tissues are reported in mg kg-1 (µg g-1) dry weight (dry wt). Water contents are 65.5%
for G. oceanicus, 72.0% for L. rudis, 72.2% for N. lapillus, 83.6% for M. edulis and 80.3%
for A. marina, leading wet wt. / dry 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 achieved at the level of individual organisms which
were independently processed and analysed. The hypothesis of normal distribution was tested
using the Lilliefors test provided in SYSTAT for Windows, Version 8.0 (Wilkinson 1998, p.
                                                4

711). Further statistical evaluation was performed using BMDP Dynamics, either non-
parametric statistics or one- and two-way analysis of variance with data screening (Dixon
1992), depending on the results of the Lilliefors test. First, global null hypotheses (equality of
means between the sites investigated) were tested either by Kruskal-Wallis test, classical
ANOVA (assuming equality of variances) or by non-classical Welch Test (not assuming
equality of variances). The adequate procedure was selected after testing equality of variances
by Levene Test. Null hypotheses were rejected at 95% significance level (P < 0.05). Second,
heterogeneity was analysed in more detail using the multiple comparison option (ZSTAT) or
the Student-Newman-Keuls Multiple Range Test (NK) (α = 0.05). The robust NK procedure
involves an adjusted significance level for each group of ordered means (Dixon 1992; p. 585).
BMDP outputs do not include values for the test statistic but only provide graphical informa-
tion (that is, means which do not differ significantly are joined to groups by vertical bars).
The advantage of this procedure is that results are readily available (see Tables 2-4), in con-
trast, for example, to outputs of pairwise t-tests (adjusted to multiple comparisons) which
would have been adequate too. Possible metal content to body size relationships were evalu-
ated using linear regression analysis (Wilkinson 1998). The significance was assessed by in-
spection of adjusted R²-values.


3. Results
The results of the QA procedure are summarised in Table 1. The analysed values for the ref-
erence materials are largely in good agreement with the certified values and the limits of de-
tection are sufficiently low for the purpose of this study, with the only exception of Pb where
gammarids proved to be below this value.
Results of the metal determinations of inshore invertebrates are compiled in Tables 2-5. Ac-
cording to results of the Lilliefors test (LIP), the hypothesis of normality has to be rejected (α
= 0.01) in a few cases only (Cd and Zn in G. oceanicus, Cd in L. rudis, Pb in M. edulis and
Cd in A. marina). Regarding the multiple comparison tests, a distinct heterogeneity between
sampling sites can be observed in many cases, e.g. for Cu and Ni in G. oceanicus (Table 2),
Cd and Ni in L. rudis (Table 3) and Cu, Cd and Pb in N. lapillus (Table 4). Furthermore, some
metals show a distinct variation with respect to the species investigated, with highest Cu, Cd
and Zn concentrations in N. lapillus.
Results of the linear regression analyses support hypotheses of clear relationships between
metal concentrations and body or shell length of individual organisms only in a few cases: viz.
Ni and Zn in G. oceanicus (Table 2; R²=0.357, P=0.007 and R²=0.187, P=0.033) as well as
Cu, Cd and Pb in L. rudis (Table 3; R²=0.225, P=0.023; R²=0.264, P=0.012 and R²=0.246,
P=0.025, respectively). A significant R²-value for Ni in N. lapillus (Table 4; R²=0.219,
P=0.029) is largely due to one outlier and will not be considered. In all other cases failure to
obtain significant relationships is mainly due to slopes not differing from zero and/or due to a
large variability of the individual metal concentrations but not to an inadequate choice of the
linear model.


4. Discussion
Interaction between size of organisms and geographical heterogeneity
It appears from Table 2-4 that for all three species investigated significant differences in body
or shell length are obtained between the Russian sites (1 and /or 2) and the Norwegian site
(3), leading to the question whether significant differences in metal concentrations in biota
                                               5

are due to a geographical heterogeneity or due to a size dependency. In all cases where no
significant linear regression between incorporated metals and length was found the answer is
in favour of a geographical heterogeneity. When a significant linear regression was obtained
for a specific site the model was used to adjust the metal concentration to the length of the
other sites under consideration. Regarding Ni in G. oceanicus from site 3 (Table 2) the ad-
justed value for a length of 19.8 mm would be 2.8 compared to the measured value of 2.4 mg
kg-1. We can thus infer that the detected significant differences are conservative and site de-
pendent. Regarding Zn we find two overlapping groups. The corresponding adjusted Zn value
for site 3 would be 65 mg kg-1, suggesting no clear differences between the sites. Regarding L.
rudis (Table 3), adjusted Cu concentrations of site 2 to a length of 16.0 mm would be 49
compared to 39 mg kg-1 and adjusted Pb concentrations of site 3 to a length of 14.2 mm 0.81
compared to 0.68 mg kg-1. In both cases we did not find significant differences but this may
eventually be the case taking the metal content to shell length dependency into account. The
significant difference found for Cd seems to be conservative as can be inferred from an ad-
justed value of 1.0 compared to 2.5 mg kg-1 for site 2.


Comparison of metal levels between species of this study
Trace metal concentrations obtained in this study and those reported for various marine in-
vertebrates from different regions are compiled in Table 6. Comparing the metal levels be-
tween species of this study we find highest Cd concentrations in the carnivorous gastropod N.
lapillus, intermediate ones in the herbivorous gastropod L. rudis and the filter feeding mussel
M. edulis and lowest concentrations in the omnivorous amphipod G. oceanicus and sediment
feeding polychate A. marina. There are two possible reasons to explain this sequence. The
first points to the different feeding strategies of the organisms investigated. However, detailed
information on the biomagnification processes for Cd in these organisms is not available.
Furthermore, gastropods may accumulate more Cd due to the relatively large portion of the
midgut gland compared to the other organisms which is an important target for this element
(Viarengo and Nott 1993). A similar sequence is found for the elements Cu and Zn.


Comparison of locations of this study
This comparison requires the consideration of interactions between size dependent metal up-
take and geographical heterogeneity as discussed above. In most cases geographical differ-
ences found become more obvious after consideration of size dependent effects. However,
there is no consistent trend of metal concentrations in biota between the Norwegian and Rus-
sian sites. In summary there appears to be more Cu in biota from the Russian site 2, but more
Ni and (to some extent) Pb in biota from the Norwegian site 3. No tendency is found for Cd
and Zn. Thus, we cannot infer a general increased bioavailability for heavy metals in the or-
ganisms from any of the sites investigated.


Comparison of Arctic data to other regions
Regarding gammaridean amphipods the data suggest somewhat enhanced Cd concentrations
in polar samples, while corresponding copper concentrations seem to be rather low. All other
elements are within the same range including uncontaminated samples from temperate re-
gions. Available data for gastropods of the genus Littorina point to some severe contamina-
tion problems in British estuaries (see notes b-f in Table 8), especially for Cu, Pb and Zn.
Compared to data from uncontaminated sites, metal concentrations in L. rudis are lower or
                                                 6

within the same range, again with the only exception of Cd. For the gastropod N. lapillus al-
most no information is available in the literature. Available data for the mussel Mytilus edulis
are rather homogeneous, not far apart from an overall median value reported in the world
mussel watch data base. Likewise, most of the reported metal concentrations in lugworms (A.
marina) are within the same range, with the only exception of some elevated levels in organ-
isms from British estuaries. A comparison of metal concentrations in invertebrates to those of
higher order animals (fish, mammals, birds) is not advisible, since the first represent whole
body concentrations while the latter are largely related to specific organs. If this is intended a
complete mass balance of elements would be required.
In general our data on Gammarus and Littorina provide to some extent further evidence for
the cadmium anomaly in invertebrates from polar waters which has been frequently discussed
in the literature (Bargagli et al. 1996; Bustamante et al. 1998; Demoreno et al. 1997; Petri and
Zauke 1993; Ritterhoff and Zauke 1997). Extreme high Cd concentrations in Antarctic crus-
taceans, related to indications of a Cu deficiency, were inferred by Petri and Zauke (1993). It
has been hypothesised, that a potential copper deficiency might be related to an increased
uptake of Cd due to a insufficient selectivity of the uptake process for the essential element
Cu.
A similar potential copper deficiency might be deduced from the relatively low values found
in G. oceanicus and L. rudis from the Barents Sea. Although some severe Ni emissions in the
Kola region (Russia) mainly from nickel smelters have been reported (Chekushin et al. 1998;
Gregurek et al. 1998; Kelley et al. 1995; Lindroos et al. 1998), we do not find indications of
an enhanced Ni availability in the marine biota studied compared to other areas.


Acknowledgements
We thank Murmansk Marine Biological Institute for invitation to Dalniye Zelentsy (Russia)
and J. Ritterhoff for his help during the field work . Travel to Murmansk was funded by Kern-
forschungszentrum Karlsruhe (Stabsabteilung Internationale Beziehungen); we thank K.
Wiendieck for his kind support. The assistance of A. Wicker and C. Pfeiffer in the analytical
work is gratefully acknowledged.


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                                                              11




     A           Barents                                B                             Barents
                                   Sea                                                                     Sea




                                                        Gu
                                                         ba
                        Reinøya




                                                             Ya
                                                                                       Guba




                                                              rn
                                         3                                             Dalnezelenetskaya




                                                                  ys
                                                              20




                                                                   hn
                                      Hornøya                                  2                 0




                                                                       ay
                                    o         o
                                 (70 22' N; 31 10' E)                           Dalniye Zelentsy        1



                                                                           a
                                                                                  o         o
                                                                               (69 07' N; 36 05' E)


         B a r e n t s

                S e a
 70 oN              A
                        B                    Vardø
     Bu
       ss
         e su
             nd
                et




                                                                           0
                                                                       0       0.5   1.0   1.5    2.0      2.5 km
 6 0o
    N     o                  o
         20 E               40 E




Fig. 1: Sampling locations for marine invertebrates in Russia (B: site 1 and 2) and Norway (A:
site 3). Note that the co-ordinates in (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 too short to be distinguished
within the chosen grain of the co-ordinates.
                                                  12

Table 1: Quality assurance using certified reference materials randomly allocated within the
determinations. Values are means ± 95% confidence intervals [mg kg-1 dry wt].
               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 ± 0.16
 Cd     3.1 ± 0.1       27     3.5 ± 0.4      0.34 ± 0.04        27      0.34 ± 0.02

 Ni     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 ± 0.04

 Zn    827 ± 78         15    852 ± 14          74 ± 2           16        76 ± 2


limit of detection: 4.7 (Cu); 0.23 (Cd); 0.5-1.0 (Ni); 0.5 (Pb) and 10 (Zn) mg kg-1 dry wt (calculated
after Büttner et al. 1980).
                                                           13

Table 2. Comparison of mean metal concentrations (mg kg-1 dry wt) in Gammarus oceanicus
from different sites of the Barents Sea (summer 1994). Means which do not differ signifi-
cantly are joined to groups by vertical bars ( ).      
                                                                                  Linear regression: Vari-
                                                                    Groups          able vs. body length
Variable          site    N      mean ± 95%CI Test                 1 2 3          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      -0.26   0.050
                   1      57        20 ± 2                                        28      -0.36   0.013
                   2      55        28 ± 3                                        35      -0.35   0.003
Cd                 1      59      0.67 ± 0.12              Z                      1.00    -0.02   0.000
                   2      58      0.85 ± 0.14                                     0.89    -0.00   0.000
                   3      20      1.01 ± 0.33                                    -0.10     0.05   0.047
Ni                 1      52        1.3 ± 0.2          NK                         2.0     -0.04   0.022
                   2      53        1.5 ± 0.2                                     1.3      0.01   0.000
                   3      17        2.4 ± 0.4                                     4.8     -0.10   0.357
Pb                 2      44            < 0.5          n.a.                         -        -        -
                   3      17            < 0.5                                       -        -        -
                   1      42            < 0.5                                       -        -        -
Zn                 1      58        61 ± 3                 Z                      64      -0.18   0.000
                   2      59        65 ± 3                                       64       0.03   0.000
                   3      20        68 ± 4                                        48       0.84   0.187

Tests of normality (LIP) and of equality of variances (LS) and means (Test; Stat)

       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)

Notes
Site: see Fig. 1 (note that the sequence follows increasing means and might differ between variables);
Test (multiple comparison tests): NK = Student-Newman-Keuls Multiple Range Test; Z = Z-statistic;
Var = variable; N: individual organisms analysed (note that N might differ between variables due to
possible failures in the multielement determination of the unique samples); CI = confidence intervals;
n.a. = not applicable; LIP = Lilliefors probabilities (2-tail); LS = Levene statistic; F = F statistic (classi-
cal ANOVA); W = Welch statistic; H = Kruskal-Wallis test statistic; P = tail probability.
                                                    14

Table 3. Comparison of mean metal concentrations (mg kg-1 dry wt) in Littorina rudis from
different sites of the Barents Sea (summer 1994). Means which do not differ significantly are
joined to groups by vertical bars ( ).
                                                                        Linear regression: Vari-
                                                            Groups        able vs. shell length
Variable         site   N      mean ± 95%CI Test           1 2          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    0.000
                  2     19        39 ± 8                                -30        4.91    0.225
Cd                2     20       2.5 ± 1.2          Z                    13        -0.75   0.264
                  3     20       7.1 ± 2.8                               28        -1.32   0.135
Ni                2     17       3.2 ± 0.8          NK                   3.7       -0.04   0.000
                  3     18       4.8 ± 1.0                              -0.7        0.34   0.059
Pb                2     17      0.66 ± 0.12         NK                  1.3        -0.04   0.065
                  3     17      0.68 ± 0.14                             1.8        -0.07   0.246
Zn                2     20        75 ± 6            NK                  52          1.63   0.000
                  3     20        85 ± 8                                104        -1.22   0.000

Tests of normality (LIP) and of equality of variances (LS) and means (Test; Stat)

       N       LIP           LS (P)          Test       Stat (P)
L      40      0.533    0.00 (0.959)           -3.02
                                             p-T
                                               (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 -2.67
                                               (0.012)
Pb     34      0.410    0.10 (0.754)       p-T -0.26
                                               (0.798)
Zn     40      0.115    0.37 (0.546)       p-T -1.98
                                               (0.055)

Notes
p-T = pooled variance t-test; M-W = Mann-Whitney test (note that N might differ between variables
due to possible failures in the multielement determination of the unique samples); otherwise as in Table
2.
                                                     15

Table 4. Comparison of mean metal concentrations (mg kg-1 dry wt) in Nucella lapillus from
different sites of the Barents Sea (summer 1994). Means which do not differ significantly are
joined to groups by vertical bars ( ).
                                                                          Linear regression: Vari-
                                                            Groups          able vs. shell lenght
Variable         site    N      mean ± 95%CI Test          1 2            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      -1.36     0.046
                  2     19         66 ± 17                                 93      -1.22     0.000
Cd                3     20         16 ± 5            NK                   -1.8      0.68     0.047
                  2     20         24 ± 5                                 12.5      0.53     0.000
Ni                3     17        1.9 ± 0.3          NK                   0.8       0.04     0.029
                  2     18        2.3 ± 0.4                               0.0       0.11     0.219
Pb                2     18        0.9 ± 0.2          NK                   0.3       0.03     0.017
                  3     17        1.9 ± 0.3                               0.8       0.04     0.019
Zn                3     20       416 ± 125           NK                   152      10.32     0.000
                  2     20       553 ± 129                                510       1.92     0.000

Tests of normality (LIP) and of equality of variances (LS) and means (Test; Stat)

       N       LIP           LS (P)           Test      Stat (P)
L      40      0.326     1.71 (0.199)         p-T    -2.23
                                                     (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    -5.14
                                                     (0.000)
Zn     40      0.052     0.75 (0.391)         p-T     1.61 (0.117)

Notes
s-T = separate variance t-test (note that N might differ between variables due to possible failures in the
multielement determination of the unique samples); otherwise as in Table 2.
                                                  16

Table 5. Metal concentrations (mg kg-1 dry wt) of inshore
invertebrates from the Barents Sea (summer 1994).

Species Variable           site    N    mean ± 95%CI LIP
M.e.      Shell length      2     20     30.0 ± 1.9       0.653
M.e.      Cu                2     20       8.9 ± 1.2      0.678
M.e.      Cd                2     20       2.0 ± 0.2      1.000
M.e.      Ni                2     20       2.9 ± 0.4      0.508
M.e.      Pb                2     16       1.6 ± 0.3      0.001
M.e.      Zn                2     20        89 ± 15       0.000
A.m.      Cu                1     10       6.8 ± 1.8      1.000
A.m.      Cd                1     10     0.34 ± 0.27      0.002
A.m.      Ni                1     10        11 ± 3        0.360
A.m.      Pb                1     10       0.8 ± 0.3      0.135
A.m.      Zn                1     10        47 ± 12       0.292
Notes
M.e.: Mytilus edulis; A.m: Arenicola marina
(note that N might differ between variables due to possible failures in the multielement determination
of the unique samples); otherwise as in Table 2.
                                                       17

Table 6. Metal concentrations in selected marine invertebrates reported in the literature
[mg kg-1 dry wt]


species              Ref   Location                           Cu        Cd        Ni        Pb        Zn
Gammarus              1    Barents Sea (site 2)               28       0.9       1.5       <1         65
oceanicus
                                            (site1)           20       0.7       1.3       <1         61
                                            (site 3)          14       1.0       2.4       <1         68
                                                       a
Gammarus salinus      2    Elbe-, Weser estuary             86-135    0.3-0.5      -      1.6-2.8    73-91
                                              a
Gammarus salinus      3    Weser estuary                      75       0.4         -       1.3        62
Gammarus locustra     4    German Bight a                     64       0.12        -       2.0        51
Gammarus 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         85
                                               b
Littorina rudis       6    Avola estuary                    333-695   0.9-1.8      -      28-44     193-552
                                               c
Littorina rudis       6    Avola estuary                    130-207   0.7-1.6      -      12-48     242-279
                                               d
Littorina littorea    7    Estuaries (GB)                   417-692    2-13     5.5-6.9    4-11     141-345
Littorina littorea    7    Estuaries (GB) e                 135-137    1.6      1.5-2.8   1.9-2.0    77-80
Littorina littorea    8    Estuaries (GB) f                  44-87    0.6-0.7 5.6-9.1     0.5-0.9    52-80
Littorina littorea    9    Shannon (Ireland)                  23         -        72         -        66
Littorina obtusata    9    Shannon (Ireland)                  18         -        27         -        65
Nucella lapillus      1    Barents Sea (site 2)               66        24       2.3       <1        553
                                            (site 3)          46        16       1.9       1.9       416
Nucella lapillus      9    Shannon (Ireland)                  45         -       5.1         -       214
Mytilus edulis        1    Barents Sea (site 2)               8.9      2.0       2.9       1.6        89
Mytilus edulis        9    Shannon (Ireland)                  7.0        -       3.0         -        88
                                               f
Mytilus edulis        8    Estuaries (GB)                    8-14     1.4-2.2   13-30     3.2-5.9   115-191
                                        a
Mytilus edulis        10   Norderney                         11-14    0.5-0.9      -      1.2-2.7   62-122
Mytilus edulis        11   Godthaab Fjord g                   8.6      1.8         -       1.7        93
Mytilus edulis        12   Island                             9.6      0.6         -       0.8       162
                                               h
Mytilus edulis        13   Chupa estuary                    4.5-4.9   4.9-5.1      -      0.5-0.7    53-67
                                    i
Mytilus edulis        14   WMW                                7.9      2.0       2.2       5.0       130
Arenicola marina      1    Barents Sea (site 1)               6.8      0.34       11       0.8        47
Arenicola marina      8    Estuaries (GB) f                  18-29    0.8-0.9    6-96     1.4-1.5   138-163
                                        a
Arenicola marina      10   Norderney                         10-30    0.4-0.9      -      1.5-2.0    81-91
Arenicola marina      15   German Wadden Sea a               8-21     0.2-0.9      -      1.0-2.4      -
                                               18

Table 6 (continued)


notes:
a
 North Sea; b Ireland (upper reach of a pollution gradient); c Irland (lower reach of a pollution
gradient); d contaminated sites (Fal, Thames); e uncontaminated sites (Teifi, Orwell); f East-
ern England (Orwell, Stour); g Greenland; h White Sea (Russia); i World Mussel Watch Data
Base (overall median value)


Ref:
1: current paper; 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: Riget (1996); 12: Olafsson
(1986); 13: Millward et al. (1999); 14: Bernds et al. (1998); 15: Lorch et al. (1990)