Trace metals in field samples of zooplankton from the Fram Strait and the Greenland Sea

ELSEVIER

The Science of the Total Environment 199 (1997) 255-270

Trace metals in field samples of zooplankton from the Fram Strait and the Greenland Sea Jiirgen Ritterhoff, Carl uon O&et&

Uniuersitiit

Oldenburg,

FB Biologie

Gerd-Peter

Zauke*

(ICBM),

2503, D-26111

Postfach

Oldenburg

Germany

Received 28 November 1996; accepted 19 February 1997

Abstract Trace metals (Cd, Pb, Ni, Cu, Zn and Hg) were evaluated in 14 zooplankton taxa collected on cruise ARK IX/Ib of RV ‘Polarstern’ to the Fram Strait and the Greenland Sea in March and April 1993. We found a substantial interspecific heterogeneity, e.g. with rather low Cd concentrations in calanoid copepods (0.1-0.7 mg kg-‘, dry wt.) but remarkably high levels in the decapod Hymenodoraglacialis(7-9 mg kg-‘) and in the amphipods Then&to abyssommand T. libellula (24-34 mg kg-‘). In general, Pb was low (< 1 mg kg-l), while some enhanced Ni concentrations were found in the ostracod Conchoeciaborealis(66-86 mg kg-‘). A comparison to world-wide reported data on marine crustaceans did not reveal any suggestions on increased metal availabilities in both areas investigated, although one might expect a transport of some metals from Siberian rivers across the pole by the Transpolar Ice Drift Stream. However, more information on accumulation strategies of zooplankton under winter 0 1997 and summer conditions is necessary before a full assessment of metals in Arctic waters will be possible. Elsevier Science B.V.

Keywords: Zooplankton;

Arctic;

Trace metals

ing more

1. Introduction Contamination of Arctic marine ecosystems with trace metals and other xenobiotics is receiv-

* Corresponding author. 004%9697/97/$17.00 PZI

SOO48-9697(97)

0 1997 Elsevier Science B.V. All rights reserved. 05457-O

attention

(AMAP,

1995;

Dietz

et al.,

1996; Hansen et al., 1996b; Macdonald and Bewers, 1996; PAME, 1996). Predominant inputs to the Arctic are from long-range transport via oceanic water mass exchanges and atmospheric processes and locally from river discharges, runoff from land and industrial emissions (Barrie et

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al., 1992; Alexander, 1995; Pacyna, 1995; Pfirman et al., 1995; Macdonald and Bewers, 1996). For example, about 6% of the total emissions of arsenic, cadmium, lead, zinc, vanadium and antimony from Eurasia is deposited in the Arctic. In summer, up to 75% of heavy metals in Arctic air originate from sources in Europe, whereas in winter 60% of metals transported to the Arctic originate from sources in the former Soviet Union. Recent estimates indicate that about 52% of the 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 Rivers Lena, Ob and Jenessei (PAME, 1996). It should be noted, however, that these rivers are pristine with respect to some metals including Pb, Cd and Hg (see review in Macdonald and Bewers, 1996). Nevertheless, drifting sea ice eventually transports chemicals from the Siberian shelves across the North Pole to the Fram Strait and the East Greenland Current (Kvambekk and Vinje, 1993; Pfirman et al., 1995). About 95% of the sea ice that leaves the Arctic Ocean is conveyed by the Transpolar Ice Drift Stream into this area, being thus the major source of fresh water to the Greenland Sea. Particular heavy metals from Siberian rivers and from atmospheric deposition may eventually become available to biota when ice is melting in the Arctic spring, especially within bands of high biological productivity at the ice edge zone (Macdonald and Bewers, 1996; PAME, 1996). The main water exchange between the Arctic Ocean and adjacent seas is due to the East Greenland Current flowing through the Fram Strait (Coachman and Aagaard, 1974) which is carrying cold water of low salinity southward on the western side of the strait. On the eastern side the Norwegian Atlantic Current and its Northern extension, the West Spitzbergen Current, is carrying warmer upper-ocean waters of high salinity northwards into the Arctic Ocean (see GSPGroup, 1990 and literature cited therein). Northward-flowing bottom water can be found beneath the current mentioned before. Both these currents make up about 78% of the inflow to the Arctic Basin (Barrie et al., 1992). The bottom

199 (1997) 255-270

water of the Greenland Sea is the coldest deepwater mass of the Nordic seas, showing highest densities. Only three copepod species, viz. C&anus glacialis (an indicator of Polar water masses), Calanus hyperboreus (an indicator of Arctic water masses) and Calanusfinmarchicus (an indicator of Atlantic water masses), usually make up 90% of the zooplankton biomass in the Greenland Sea (Hirche et al., 1994). Zooplankton plays a major role in the Arctic food web with copepods, euphausiids and amphipods being important food resources for marine mammals, birds and fish (e.g. Smith and Schnack-Schiel, 1990; Percy, 1993; Nilssen et al., 1995a,b and literature cited therein). Thus, zooplankton organisms may contribute to the transfer of metals to higher trophic levels and have been chosen, among others, as recommended organisms in baseline studies for the marine environment, for example, within the scope of the Arctic Monitoring and Assessment Programme (AMAP, 1995). Before using organisms as biomonitors of environmental metal availabilities, information is required on their accumulation strategies and on corresponding cation homeostasis mechanisms, including potentials for detoxification (e.g. Rainbow et al., 1990; Rainbow, 1993; Viarengo and Nott, 1993; Zauke et al., 1995; Zauke et al., 1996b). Investigations on the time course of uptake and clearance of metals in organisms, in relation to external metal exposures, are a first step to assess the significance of metals in aquatic systems. They provide the experimental basis for estimation of kinetic parameters of compartment models and first hypotheses on underlying accumulation strategies (van Hattum et al., 1989; Matis et al., 1991; Timmermans et al., 1992; Xu and Pascoe, 1993; Zauke et al., 1995; Ritterhoff et al., 1996). Corresponding investigations have been performed on cruise ARK IX/lb of RV ‘Polarstern’ to the Fram Strait and the Greenland Sea (parallel to field sampling which is the focus of this presentation). Toxicokinetic experiments and concentration-dependent uptake studies have been carried out using the copepods Calanus hyperboreus, C. jinmarchicus and Metridia longa and the amphipod Themisto abyssoium (Ritterhoff and

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Zauke, 1997; Ritterhoff and Zauke, submitted). Results obtained encourage us to recommend the collectives investigated as potential biomonitors for Cu, Pb and, to some extent, for Zn, since they show a tendency for net accumulation. In contrast, Cd is not taken up significantly, at least regarding the animal’s life-history status by the end of the Arctic winter. Additional results from studies on the influence of body length and life history status on metal concentrations in T. abyssorum, T. libellula and C. hyperboreus suggest only to consider adult individuals for biomontoring purposes (Ritterhoff and Zauke, in press). Since important preconditions are met to utilise ecologically relevant zooplankton organisms from Arctic waters as biomonitors, we report in the present paper data on Cd, Pb, Cu, Zn, Ni and Hg in 14 sorted zooplankton collectives from the Fram Strait and the Greenland Sea. The organisms considered cover a wide range of taxa. Results are discussed with respect to interspecific, spatial and seasonal heterogeneity and to potential metabolic requirements, inferred from literature data on decapod crustaceans. It should be stressed, however, that information on some elements (Cd, Ni, Hg) and on some zooplankton taxa needs further substantiation due to lack of experimental data on accumulation strategies as mentioned above. 2. Material

and methods

2.1. Sampling and sample preparation

Zooplankton samples were collected on Polarstern cruise ARK IX/lb to the Fram Strait and the Greenland Sea in March and April 1993 mainly along transects on 24 stations at 79” N and 75” N (Fig. 1). More information on the cruise is available in Eicken and Meincke, 1994. Samples were taken with a vertically towed bongo net from about 1500 m depth to the surface (mesh size 200 pm and 300 pm; hauling at 0.3 m s-l> and by trawling an oblique rectangular midwater trawl (RMT 1 + 8) from 1000 m depth to the surface at 2 kn (mesh size 200 pm and 300 pm; hauling at 0.5 m s-l>. On board ship, the animals were transferred to polyethylene buckets containing

199 (1997) 255-270

257

seawater from different stations (depths > 500 m) and kept alive at least for 6 h at 0°C to allow for defecation (which is probably not necessary at all, see results and discussion). Subsequently, the samples, still alive, were sorted under a binocular microscope, shortly rinsed with double-distilled water, dried on good quality filter paper and immediately frozen at - 80°C in polypropylene and polystyrol containers. The risk of contamination was largely reduced by the following preventive measures. Firstly, the animals were almost always kept in seawater and secondly the absence of any contaminating particles in the samples such as paint particles, tar lumps or plastic was guaranteed by close visual examination of each specimen collected. According to results on the influence of lifehistory status on metal accumulation reported in Ritterhoff and Zauke (in press) only adult organisms were considered in this study. Details on the organisms collected are summarised in Table 1. We use the expression ‘collective’ as the basic unit of observation throughout this paper to emphasise that a strict random sampling and a definite (viz. destructive) species determination of all specimen collected is not possible in any case (Zauke et al., 1996a; Ritterhoff and Zauke, 1997). 2.2. Analytical procedures

Upon arrival at the laboratory the samples were immediately lyophilised. The organisms were subsequently homogenised using a boron carbide mortar and pestle, only the copepods were processed as whole animals. Details of the analytical procedures are described in Petri and Zauke (1993) and Zauke et al. (1996a). Aliquots of about 10 mg dried material were digested for 1 h at 96°C with 50 ,ul HNO, (70-71%, Baker InstraAnalysed) in 1.5 ml Eppendorf reaction tubes (safe lock). The elements Cd, Pb, Ni and Cu were determined using sequential multielement graphite tube atomic absorption spectroscopy (Varian Techtron, AA-975, GTA-95, platform atomisation). Zn was determined in an airacetylene flame using a manual micro-injection method (100 ~1 sample volume). For all determinations deuterium background correction was ap-

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Table 1 General information of zooplankton organisms sampled during cruise ARK IX/lb Greenland Sea (March 1993).

199 (1997) 255-270

of RV ‘Polarstem’ to the Fram Strait and the

Species

T

Sampling stations*

Themisto abyssorum (Boeck, 1870) Them&o libellula (Mandt, 1867) Calanusfinmarchicus (Gunnerus, 1765) Calanus glacialis Jaschnow, 1955 Calanus hyperboreus Kroyer, 1838 Euchaeta barbata Brady, 1883 Euchaeta glacialis (Hansen, 1886) Euchaeta norvegica (Boeck, 1872) Metridia longa (Lubbock, 1854) Eukrohnia hamnta (Mobius, 1875) Hymenodora glacialis (Buchholz, 1874) Meganyctiphanes norvegica (M. Sars, 1857) Thysanoessa inermis (Kroyer, 1846) Conchoecia borealis G.O. Sars, 1865

A All except 41,43,46,53,61,66,69 A All except 13,15,17,23,28,29,61,66, 19 C All except 41,49,51,53,66 C 28,29 C All except 41,53,66 C 43,53,67,69 C 34,46,49,51,56,67 C 34,46,49,51,56,67 C 23,28,34,36,39,43,49,51,54,.56, 61,69 Ch 17,34,36,39,43,56,65 D All except 13,17,20,34,39,46,49,67 E 34,56 E 34,46,56,67 0 18,20,34,39,43,46,49,54,56,61,65, 67

F

References

Car Car Omn Omn Omn Car Car Car Omn Car Car Her Her Car

Macdonald and Sprague (1988) Macdonald and Sprague (1988) Harris (1996) Harris (1996) Harris (1996) Clarke and Peck (1991) Clarke and Peck (1991) Clarke and Peck (1991) Hansen et al. (1996a) Oresland (1995) Chace (1986) Paul et al. (1990) Paul et al. (1990) Gruner et al. (1993)

T, taxon (A, amphipods; C, copepods; Ch, chaetognaths; D, decapods; E, euphausiids; 0, ostracods). ‘Refers to station numbers in Fig. 1; F, main feeding strategy (car, carnivorous; her, herbivorous; omn, omnivorous).

Abbreuiations:

plied. Regarding Hg, aliquots of about 10 mg dried material were digested for 1 h at 96°C with 50 ~1 HNO, (70-71%, Baker Instra-Analysed) and 50 ~1 HCl(37%, Riedel de Haen, p.a.> in 1.5

ml Eppendorf reaction tubes (safe twist). Hg determinations involved reduction of the digest with SnCl, (10 g/100 ml solution of 3.7% Ha>, evaporation of Hg by application of nitrogen (5.0) for

Fig. 1. Stations for sampling of zooplankton collectives during cruise ARK IX/lb the Greenland Sea (O), March 1993, see Table 1 and text for more details.

of RV ‘Polarstern’ to the Fram Strait (m) and

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3 min and subsequent amalgamation on a Pt/Aunet (Varian Techtron, MK II, AA 975). The net was electrically heated after 3 min to deliberate the mercury collected. Standard solutions were stabilised with potassium dichromate (p.a.). Quality assurance was performed in line with German GLP regulations. The precision and validity was evaluated using three certified reference materials which were randomly allocated within the determinations (Table 2). Limits of detection were calculated following DIN 32645, 1994 and Biittner et al., 1980. All metal concentrations in biological materials are expressed as mg kg-l (pgg-‘) drywt. 2.3. Statistical procedures

The hypothesis of normal distribution was tested using the Lilliefors test provided in SYSTAT for Windows (Wilkinson et al., 1992, pp. 495, 718). Since this hypothesis had not to be rejected in most cases ((Y = 0.01) further statistical evaluation was performed using BMDP PC90, program 7d, (Dixon et al., 1990). First, global null hypotheses (equality of means) were tested either by 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 Table 2 Quality assurance using certified reference confidence intervals (mg kg-’ dry wt.).

Cd Pb CU Zn Ni Hs Hg

3.7 f 0.1 0.5 * 0.2 64.1 + 1.4 782 + 63 1.03 * 0.21

randomly

199 (1997) 255-270

Certified 3.5 0.48 63.0 852 1.03 -

Analysed * 0.4 f 0.04 f 3.5 * 14 +0.19

0.35 f 0.02 2.1 * 0.2 9.8 f 0.30 72 kl 1.2 * 0.17 0.18 * 0.01 0.784 f 0.034"

259

rejected at 95% significance level (P < 0.05). Second, heterogeneity was analysed in more detail using the Student-Newman-Keuls Multiple Range Test ((Y = 0.05). The robust NK procedure involves an adjusted significance level for each group of ordered means. 3. Results and discussion 3.1. Quality assurance

Analysed values obtained for reference materials generally are in good agreement with the certified ones (Table 2). Limits of detection proved to be adequate for the range of metal concentrations found in this study. The procedure of Biittner et al. (1980) yielded almost the same results as DIN 32645 displayed in Table 2. 3.2. Metal concentrations taxa

in different zooplankton

Metal concentrations detected in different zooplankton taxa from the Fram Strait and the Greenland Sea are listed in Tables 3 and 4. The Lilliefors probabilities (LIP) suggest, in most cases, that the hypothesis of a normal distribution cannot be rejected at the 99% significance level, while global null hypotheses (equality of means) have to be rejected in all cases (with tail probabilallocated

within

the determinations.

CRM 278 (Mussel tissue)

NET SRM 1566 (Oyster tissue) Analysed

materials

Total Environment

Values

are means

~95%

NIST SRM 1572 (Citrus leaves) Certified

Analysed

0.34 f 0.02 1.91+ 0.04 9.6 + 0.16 76 +2 (1.0) 0.19 f 0.01 0.798+ 0.074a

Numbers of independent determinations: 27 for Cd to Ni and 35 for Hg. aHg in NRC Dorm-l (dogfish muscle). bBelow limit of detection: viz. 0.10 mg Cd kg-‘; 0.3 mg Pb kg-‘; 1.7 mg Cu kg-‘; kg-’ ; (dry wt.; calculated after DIN 32645).

Certified

b

12.9 f 1.1 16.3 & 0.7 30 +2 0.7 + 0.2

4.8 mg Zn kg-‘;

1.0 mg Ni kg-’

0.03 + 0.01 13.3 + 2.4 16.5 + 1.0 29 +2 0.6 f 0.4

; 0.02 mg Hg

260 Table Metal

J. Ritterhofl 3 concentrations

(mg kg-’

Sample

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dly wt.) in zooplankton T

Mean

from + 95%CI

the Fram

strait N

(Polarstern, LIP

199 (1997) 255-270

ARK

IX/lb,

C. C. M. C. C. H. T T.

finmarchicus glacialis longa hyperboreus borealis glacialis libellula abyssolum

0.32 0.63 0.71 0.75 1.21 9.20 23.5 27.7

Pb

H. C. C. C. T. M. T C.

glacialis finmarchicus glacialis hyperboreus libellula longa abyssorum borealis

< 0.3 < 0.3 < 0.3 0.3 0.5 0.6 1.2 3.1

T. H. C. T. C. C. M. C.

libellula glacialis jinmarchicus abyssolzlm glacialis hyperboreus longa borealis

1.6 1.9 3.0 3.6 4.3 11.4 19.7 65.8

Ni

Test of global null hypotheses: Cd Ls: 39.1 (P = 0.000); Pb Ls: 9.50 (P = 0.000); Ni Ls: 10.8 (P = 0.000);

ws: 119 WS: 27.2 WS: 52.0

+ ? + + f f * +

0.04 0.09 0.05 0.06 0.17 4.44 4.76 3.22

26 8 9 28 7 12 14 26

0.123 0.784 0.728 0.837 1.000 0.168 0.732 0.471

+ * + + +

0.1 0.3 0.3 0.2 1.7

10 27 8 29 13 9 26 7

0.021 0.260 0.582 1.000 0.301

k + + k f & + i

0.4 0.9 0.5 0.5 1.0 1.5 4.4 13.9

13 12 26 25 8 29 9 7

0.953 0.273 0.776 0.162 0.923 0.503 0.502 0.179

-

(P = 0.000; d.f. = 7,35) (P = 0.000; d.f. = 7,35) (P = 0.000; d.f. = 7,34)

CU

C. C. C. M. H. T. T. C.

glacialis finmarchicus hyperboreus longa glacialis abyssorum libellula borealis

4.0 4.5 5.6 7.5 12.4 21.8 23.0 43.0

+ + f + & + i: +

Zn

H. T. C. T. C. C. M. C.

glacialis libellula glacialis abyssorum Jinmarchicus hyperboreus longa borealis

52+11 61*6 79 + 86 + 93 + 104 f 351+ 358 k

0.5 0.2 1.2 2.5 5.7 2.5 5.3 7.1

8 28 27 9 12 26 14 7

0.120 0.226 0.618 0.000 0.104 0.015 0.340 0.275

7 5 8 8 58 49

11 14 8 26 27 29 8 7

0.048 1.000 0.040 0.349 0.730 0.043 0.108 0.834

1993)

Groups 1

Cd

March

2

3

4

J. Ritterhofi Table

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199 (1997)

255-270

261

3 (Continued)

H. C. T. C. C. T. C. M.

Test of global cu LS: Zn Ls: Ls: Hs

glacialis hyperboreus libellula glacialis borealis abyssorum jinmarchicus longa null 18.3 6.96 10.3

hypotheses: (P = 0.000); (P = 0.000); (P = o.ooo>;

T

Mean

D C A C 0 A C C

0.13 0.31 0.32 0.42 0.45 0.54 0.56 0.68

f f + + + + + f

k 95%CI

N

LIP

1

0.05 0.04 0.09 0.19 0.27 0.05 0.12 0.28

8 29 13 8 7 25 28 9

1.000 0.374 0.013 0.705 0.712 0.084 0.443 0.963

I I I

2

3

4

I

I

WS: 60.1 (P = 0.000; d.f. = 7,34) WS: 54.6 (P = 0.000; d.f. = 7,35) WS: 22.7 (P = 0.000; d.f. = 7,33)

Bars ( 1) indicate groups identified by the Student-Newman-Keuls Multiple Range Test according to the BMDP output. Abbreviations: N, independent subsamples, analysed in different series of determination; LIP, Lilliefors probability; LS, Lcvene statistic; WS, Welch statistic; P, tail probability (corresponding null hypotheses are rejected when P < 0.05); d.f., degrees of freedom (for LS, strata-l; total of determinations-strata); otherwise as in Table 1.

ities for the Welch statistics being below 0.05, respectively). The results indicate a substantial interspecific heterogeneity of metal concentrations. The identification of different groups by the NK procedure reveals rather complex patterns of metal concentrations regarding different zooplankton collectives. Detected differences in metal levels are remarkable, with Cd showing factors of more than 100, Ni more than 50, Pb up to 10, Cu more than 10 and Zn and Hg of 5-10, comparing lowest and highest metal concentrations for corresponding zooplankton collectives. The variability found in this study, ranging from limits of detection to rather high levels, may be regarded as an a posteriori quality assurance of the sample preparation on board ship (Zauke and Petri, 1993). Because of the methods used, possible contamination could only by chance have affected subsamples, but not specific zooplankton taxa. In general, Cd concentrations are rather low in copepods (0.1-0.7 mg kg-l) but remarkable high in decapods (7-9 mg kg-‘) and amphipods (24-34 mg kg-‘) from both areas investigated. The same is true for copper. Regarding the other metals, such patterns could not be discerned. For most collectives analysed, Pb concentrations are rather low, being in many cases close to the limit of detection. Only for the ostracod Conchoecia bore-

alis elevated Pb levels are noted. In that species we have likewise found elevated concentrations of Cu, Zn and Ni, with Ni levels reaching 86 mg kg-l dry wt. in theGreenland Sea. These levels can be regarded as one of the highest concentrations reported for marine invertebrates (see below). Thus, C. borealis must have developed a special accumulation and detoxification strategy for this element which merits further investigations. In some terrestrial plants hyperaccumulation of Ni is regarded as a potential defence mechanisms against grazing (Martens and Boyd, 1994) and it would be interesting to clarify whether such phenomenon also exist in zooplankton. Euphausiids generally show rather low metal concentrations, with the exception of Cu. A similar situation is noted for the chaetognath Eukrohnia hama ta . In any case, results of multicomparison tests are dependent on the a priori scientific questions involved. We have been dealing so far with the problem of interspecific heterogeneity regarding the complete set of taxa. Because of the enormous variability found in this study it is impossible to detect, for example, smaller differences between the copepods investigated. Such detailed analysis would be, however, recommended due to the enormous ecological relevance of this group in Arctic waters. Thus, results of the NK-proce-

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heterogeneity between copepods which was not the case for the complete dataset. Our study and results reported in the literature

dure considering these collectives alone are summarised in Table 5. Regarding this subset of data, it was possible to detect a substantial interspecific Table Metal

4 concentrations

(mg kg-l

Sample

dry wt.) in zooplankton T

Mean

+ 95%CI

from

the Greenland N

LIP

Sea (Polarstern,

Pb

Ni

T E. E. E. C. M. M. C. E. C. H. T. i?

inermis glacialis norvq$ca barbata finmarchicus norvegica longa hyperboreus hamata borealis glacialis abyssorum libellula

E C C C C E C C Ch 0 D A A

M. T. E. H. E. C. C. E. E. T. M. T. C.

norveg&a inermis norves’ca glacialis glacialis jinmarchicus hyperboreus hamata barbata libellula longa abyssonrm borealis

E E C D C C C Ch C A C A 0

< < < < < < < < <

0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.3 0.4 0.5 1.0 2.3

E. T. H. T. E. C. M. T. E. E. C. M. C.

hamata inermis glacialis libellula glacialis jinmarchicus norvegica abyssoncm norvegica barbata hyperboreus longa borealis

Ch E D A C C E A C C C C 0

< 1.0 1.1 1.4 1.9 2.1 2.6 2.6 3.0 3.0 3.9 9.7 15.6 85.9

Test of global null hypotheses: Cd Ls: 53.5 (P = 0.000); Pb LS: 31.6 (P = 0.000); Ni LS: 51.8 (P = 0.000);

< 0.10 0.12 0.13 0.16 0.27 0.44 0.61 0.69 1.09 1.53 6.74 28.2 33.8

WS: 215 WS: 34.5 ws: 117

0.02 0.07 0.07 0.03 0.10 0.08 0.04 0.11 0.10 1.45 2.60 7.07

12 .23 19 11 36 19 24 84 27 34 29 45 47

+ f + +

0.1 0.1 0.1 0.6

17 12 19 30 22 36 80 26 10 48 22 44 32

+ * + + f + + + * + & +

0.4 0.3 0.3 0.4 0.3 0.5 0.4 0.9 1.0 0.9 1.8 10.2

27 12 30 47 22 35 19 44 19 11 81 24 34

+ f f f + k + f f f + f

0.568 0.001 0.144 0.032 0.023 0.392 0.011 0.129 0.158 0.348 0.031 0.000 -

0.082 0.180 0.156 0.069

0.569 0.246 0.068 0.013 0.173 0.054 0.099 0.614 1.000 0.019 0.693 0.000

(P = 0.000; d.f. = 12,117) (P = 0.000; d.f. = 12,108) (P = 0.000; d.f. = 12,108)

ARK

IX/lb,

March

1993)

5

6

Groups 1

Cd

199 (1997) 255-270

2

3

4

7

J. RitterhofiS Table

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263

4 (Continued)

-

T

Mean

+ 95%CI

-

N

LIP

cu

E. hamata C. jinmarchicus C. hyperboreus E. barbata E. norvegica E. glacialis M. longa H. glaciulis I: abyssorum T. libellula M. noluegica T. inermis C. borealis

Cb C C C C C C D A A E E 0

3.2 3.8 4.4 4.5 4.5 4.7 5.9 15.6 23.5 26.2 35.2 38.5 50.7

0.3 0.3 0.2 0.9 0.6 0.5 0.4 3.0 1.3 4.6 5.3 6.3 5.5

26 35 84 11 19 23 23 29 45 48 19 12 34

0.073 0.420 0.083 0.058 0.417 0.315 0.363 0.878 0.507 0.111 0.071 0.916 0.073

Zn

H. M. T. E. T. C. C. i? E. E. E. C. M.

glacialis norvegica libellula hamata inermis finmarchicus hyperboreus abyssorum glacialis norvegica barbata borealis longa

D E A Ch E C C A C C C 0 C

37 * 2 42_+2 61+3 69 t 4 78 f 9 86 f 6 88 k 4 92 f 6 157 i: 12 172 + 11 225 * 38 337 + 24 389 f 34

29 19 44 26 12 35 84 45 23 19 11 30 24

0.746 0.466 0.213 0.050 0.423 0.001 0.042 0.035 0.449 0.720 0.070 0.010 0.265

H. T M. C. T T. E. E. C. E. C. E. M.

glacialis inermis norvegica hyperboreus libellula abyssomm hamata barbata borealis glacialis finmarchicus nomegica longa

D E E C A A Ch C 0 C C C C

0.06 0.12 0.13 0.20 0.23 0.26 0.26 0.27 0.30 0.30 0.35 0.35 0.50

25 11 19 69 48 43 27 11 34 23 37 19 23

0.907 0.040 0.000 0.011 0.068 0.001 0.000 0.606 0.499 0.612 0.017 0.407 0.027

Hg

199 (1997) 255-270

Test of global null hypotheses: cu Ls: 30.4 (P = 0.000); Zn LS: 36.1 (P = 0.000); LS: 21.6 (P = 0.000); Hg Bars ( 1) indicate groups identified see text for more details. Notation as in Table 1 and Table

ws: 137 WS: 246 WS: 45.5

5 * f * + f t k f f + f &

k + + + k f k k + f * + +

0.01 0.04 0.04 0.02 0.03 0.03 0.07 0.06 0.06 0.05 0.11 0.07 0.15

1

I I

2

3

i

I

4

5

6

7

I I I

I

I

I I

I

I

I

I

I

I

I

(P = 0.000; d.f. = 12,106) (P = 0.000; d.f. = 12,107) (P = 0.000; d.f. = 12,105)

by the Student-Newman-Keuls

Multiple

Range

Test according

to the BMDP

output

(a = 0.05);

3.

(e.g. Petri and Zauke, 1993; Zauke et al., 1996a and information compiled in Table 7) strongly suggest that data based on poorly characterised

mixed samples or the entire zooplankton compartment should not be used in biomonitoring programs or in modelling of metal fluxes in the

264

J. Ritterhoff;

Table 5 Multiple comparisons Fram

Strait

of metals

G.-P. Zauke

regarding

sample

C. C. M. C.

finmarchicus glacialis longa hyperboreus

Pb

C. C. C. M.

Ni

Science of the Total Environment

Greenland 2

Sea sample

3 E. E. E. C. M. C.

glacialis noruegica barbata finmarchicus longa hyperboreus

finmarchicus glacialis hyperboreus longa

Pb

E. E. C. C. E. M.

norvegica glacialis jinmarchicus hyperboreus barbata longa

C. C. C. M.

finmarchicus glacialis hyperboreus longa

Ni

E. C. E. E. C. M.

glacialis Jinmarchicus norvegica barbata hyperboreus longa

CU

C. C. C. M.

glacialis jinmarchicus hyperboreus longa

al

C. C. E. E. E. M.

finmarchicus hyperboreus barbata noruegica glacialis longa

Zn

C. C. C. M.

glacialis finmarchicus hyperboreus longa

Zn

C. C. E. E. E. M.

finmarchicus hyperboreus glacialis norve@‘ca barbata longa

Hg

C. C. C. M.

hyperboreus glacialis jinmarchicus longa

Hg

C. E. E. C. E. M.

hyperboreus barbata glacialis finmarchicus norvegica longa

null hypotheses* 125 (P = 0.000; 4.52 (P = 0.013; 65.0 (P = 0.000; 11.0 (P = 0.000; 41.4 (P = 0.000; 7.75 (P = 0.002;

I I I

I

I

322) 3,221 3,181 3,20) 3,23) 3,181

WS: WS: WS: WS: WS: WS:

Groups 1

Cd

Test of global Cd WS: Pb WS: Ni WS: cu WS: Zn WS: WS: Hg

199 (1997) 255-270

only copepods

Groups 1

Cd

/The

I I

2

3

4

: d.f. d.f. d.f. d.f. d.f. d.f.

= = = = = =

158 7.2 86.1 15.7 128 8.7

(P (P (P (P (P (P

= = = = = =

Bars ( 1) indicate groups identified by the Student-Newman-Keuls see test and Table 3 for more details. Notation as in Tables 1 and 3. * Levene statistics > 2.63 (P < 0.025).

0.000; 0.000; 0.000; 0.000; 0.000; 0.000;

d.f. d.f. d.f. d.f. d.f. d.f.

= = = = = =

Multiple

5,531 5,48) 5,52) 5,49) 548) 5,52) Range

Test according

to the BMDP

output

((Y = 0.05);

.I. Ritterhofl

G.-P. Zauke

/ The Science of the Total Environment

Ocean. Such a holistic view, although promising with respect to ecological modelling approaches (PRISMA, 19941, must be regarded as inadequate, even when treating only rather narrow taxonomic groups like calanoid copepods. 3.3. Spatial and seasonal heterogeneity

The first hypotheses on spatial heterogeneities of metals in organisms may be derived from a comparison of organisms from the Fram Strait and the Greenland Sea. It is, however, not possible to discern a consistent pattern or general trend from the results given in Table 6. In many cases (about 66% of the comparisons) no significant differences between these areas are obvious. Only for Calanus jinmarchicus and C. hyperboreus we recognise significant differences for most metals analysed. In all these cases, metal concentrations in organisms from the Fram Strait are somewhat higher compared to those from the Greenland Sea, with the only exception of Cd in Conchoecia borealis, where the opposite is true. A more detailed evaluation comparing different stations within any of these areas is prevented by the experimental design of this study. Since it was only possible to obtain one bongo net or one RMT haul on each sampling station, no true replicates sensu Hurlbert (1984) exist for this Table 6 Comparison of metal concentrations in zooplankton samples March 1993); T- and P-values obtained from &test (BMDP Sample

Cd

C. finmarchicus

T-value P-value T-value P-value T-value P-value T-value P-value T-value P-value T-value P-value T-value P-value

C. hyperboreus M. longa C. borealis H. glacialis T abyssorum T. libellula Notation

as in Table

1.

2.48 0.016 1.71 0.090 1.52 0.139 -3.59 0.004 1.46 0.151 0.54 0.590 - 0.89 0.375

199 (1997) 255-270

level of consideration. The independent subsamples prepared on each station have to be regarded as evaluation units sensu Hurlbert and White (1993). Consequently, we focus on larger regions as units of investigation, regarding different stations as replicates, a situation which will often be the case in biological oceanography. This problem of scaling is treated in more detail in Zauke et al. (1996b), taking Cd in gammaridean amphipods as an example. As a consequence, no attempts can be made to differentiate between various water masses (viz. Atlantic and polar water bodies within the Fram Strait) to address, for example, potential influences of sea ice drift on metal availabilities for zooplankton organisms (see below). Some preliminary hypotheses on seasonal heterogeneity of metals in zooplankton can be derived by comparison of our results (obtained from organisms collected from water depths down to 1500 m by the end of the Arctic winter) to results of Pohl (1992) which were obtained from organisms collected from surface layers during the Arctic summer (July 1990). The most interesting feature is that Pohl (1992) found elevated concentrations of Cd in Calanus hyperboreus and C. jinmarchicus (Table 7) which were about one order of magnitude higher compared to results presented in this study (Tables 3 and 4). Possible explanations for the seasonal differences detected

from the Fram Strait and the Greenland PC-90); see text for more details.

Pb

0.96 0.344 1.23 0.225

2.81 0.007 0.99 0.324

265

Sea (Polarstern,

ARK

IX/lb,

Ni

cu

Zn

Hg

2.17 0.034 2.43 0.019 1.96 0.074 - 1.75 0.088 1.31 0.199 2.33 0.023 - 0.26 0.796

3.49 0.001 5.19 0.000 1.40 0.198 - 1.25 0.219 - 1.14 0.263 -0.37 0.709 - 0.09 0.929

1.52 0.133 3.20 0.003 - 1.19 0.242 0.80 0.430 2.94 0.014 - 1.14 0.258 - 1.22 0.228

2.63 0.011 4.61 0.000 1.32 0.197 1.90 0.065 3.11 0.015 9.25 0.000 1.67 0.099

266 Table Metal

J. Ritterhofl 7 concentrations

(mg kg-l

G.-P. Zauke

/ The Science of the Total Environment

dry wt.) in zooplankton

from

different

Species

Taxon

Region

Cd

Themisto abyssorum Themisto compressa Themisto gaudichaudii Themisto gaudichaudii Themistopacijica Themisto libellula Themisto libellula Themisto libellula Phrosina semilunata Phronima sedentaria Hyperia sp. Eusirus propeperdentatus Paraceradocus gibber Calanusplumchrus Calanus cristatus Calanus finmarch. /helgol.” Calanus finmarch. / helgol.” Calanus finmarch. /helgoLa Calanw$nmarchicus Calanus~nmarchicus Calanusj?nmarchicus Calanus hyperboreus Calanus hyperboreus Chorismus antarcticus Notocrangon antarcticus Systellaspis debilis

A A A A A A A A A A A A A C C C C C C C C C C D D D

12-20 70 I9 53 10 9.1 11 9-18 6.6 2.0-8.8 51 9.5 3.8 8.8 2.4 1.8 3.2 10.9 6.6 8.9 1.0 4.0 2.7

Meganyctiphanes norvegica Meganyctiphanes norvegica Meganyctiphanes norvegica Meganyctiphanes norvegica Meganyctiphanes norvegica Thysanoessa longipes Euphausia superba Euphausia superba Euphausia superba Euphausia superba Euphausia superba Euphausia pacifica

E E E E E E E E E E E E

Canadian Arctic NE Atlantic Antarctic Antarctic N Pacific Bering Sea Canadian Arctic West Greenland Mediterranean NW Mediterranean Northern North Sea Antarctic Peninsula Antarctic Peninsula N Pacific Behring Sea Southern North Sea Central North Sea Northern North Sea Greenland Sea Fram Strait West Greenland Greenland Sea Fram Strait Weddell Sea, Antarctic13 Weddell Sea, Antarctic13 Atlantic (African coast) Firth of Clyde NE Atlantic NE Atlantic Atlantic (Spain) Mediterranean Bering Sea Antarctic Peninsula Scotia Sea, Antarctic Antarctic Ocean Weddell Sea, Antarctic Signy Is., Antarctic N Pacific

“C. finmarchicus/C.

helgolandicus.

Notation

as in Table

11-32 1.1 0.7 0.4 0.3 1.3 0.4-1.1 0.3 0.7 1.9 3.5 0.8 0.2-2.2

regions CU

199 (1997) 255-270

of the world Zn

39 28 31

76 59 66

Pb

-

-

24 18-35 26 107 53 7.1 6.6 7.0 8.4 7.9 4.7 6.2 93 67 26-83 36 58 72 66 81 29 54 66 54

150 108-197 72 49 63 132 121 129 123 70 152 176

1.8 0.4 1.4 1.0 1.0 1.0 2.0 0.5

80 59 44 46 42-93

0.5 0.6 1.6 0.8 -

43 102 97 104 85 59-88 44 41 33 68 96-195

0.2 1.5 0.2 0.3 -

References Macdonald and Sprague (1988) Rainbow (1989) Rainbow (1989) Rainbow (1989) Hamanaka and Tsujita (1981) Hamanaka and Ogi (1984) Macdonald and Sprague (1988) Dietz et al. (1996) Fowler and Benayoun (1974) Romeo et al. (1992) Zauke et al. (1996a) Petri and Zauke (1993) Petri and Zauke (1993) Hamanaka and Tsujita (1981) Hamanaka and Tsujita (1981) Zauke et al. (1996a) Zauke et al. (1996a) Zauke et al. (1996a) Pohl(1992) Pohl(1992) Dietz et al. (1996) Pohl(1992) Pohl(1992) Petri and Zauke (1993) Petri and Zauke (1993) Ridout et al. (1985) Rainbow (1989) Rainbow (1989) Ridout et al. (1989) Leatherland et al. (1973) Romeo et al. (1992) Hamanaka and Tsujita (1981) Locarnini and Presley (1995) Stoeppler and Brandt (1979) Yamamoto et al. (1987) Petri and Zauke (1993) Rainbow (1989) Hamanaka and Tsujita (1981)

1.

in field samples from both studies may be related either to changing accumulation strategies of the copepod species involved or to changing bioavailabilities of water born or particle bound cadmium in this area. Since we have not found any relevant uptake of water born cadmium in bioaccumulation experiments performed during the winter cruise (Rit-

terhoff and Zauke, 1997; Ritterhoff and Zauke, submitted), a first hypothesis would involve a switch of the copepod’s accumulation strategy after overwintering from regulation to net accumulation. As a consequence they would accumulate Cd in the summer season, leading to relatively high levels reported by Pohl (1992). In winter no further Cd would be taken up and the

J. Ritterhoft; G.-P. Zauke /The Science of the Total Environment 199 (1997) 255-270

body burden of the copepods would drop down to relatively low levels observed in this study, provided that a relevant depuration occurs. A second hypotheses would involve a significant Cd absorption in copepods from food during summer when they intensively feed on phytoplankton, while the food uptake path is irrelevant in winter. During that time calanoid copepods survive over winter in a diapause-like condition and are unable to feed, since their mid-gut epithelium and their digestive enzymes are reduced (Hallberg and Hirche, 1980; Tande and Slagstad, 1982; Hirche, 1983; Hirche, 1991; Hirche, 1996). Thus, they will be unable to take up any more Cd during winter. However, only if a strong depuration occurs it would be possible that Cd levels drop down significantly because the organisms will also loose body weight due to the consumption of their fat reserves laid down in the summer. A third hypothesis would involve an increased availability of water born cadmium related to drifting sea ice which may transport pollutants from East Siberian rivers across the pole to the Fram Strait (see introduction). Such an increased availability might occur even if those rivers are not regarded to be polluted by this element (Macdonald and Bewers, 1996). In any case, such material may become available to copepods in summer (then living in the surface water layers) due to melting of ice, while it will be not available for them in winter when they live in water depth below 800 m (own observations and Richter, 1995). Only after these hypotheses have been tested (which must be directed to future studies) a full assessment of trace metals in zooplankton organisms from Arctic waters will be possible. 3.4. Metal concentrations in marine crustaceansfrom different regions

Trace metal concentrations reported for marine crustaceans from different regions of the world are compiled in Table 7. Data regarding mixed zooplankton without addressing, at least, higher taxa are not considered, due to the enormous variability which has to be expected (see above). It should be stressed that interspecific comparisons may be of limited value unless a

267

calibration and assessment of accumulation strategies has been done (Rainbow, 1993; Zauke et al., 1996b). Unfortunately, such calibration is neglected in most field studies due to the substantial effort associated with this approach. However, the following tentative conclusions may be drawn. In general, Cd concentrations in marine amphipods show a remarkable variability. Among this taxon, adult hyperiid amphipods of the genus Themisto exhibit atypically high concentrations of Cd (reaching up to 70 mg kg-‘) which belong to the highest values reported in literature for marine invertebrates (Tables 3, 4 and 7). High Cd levels are also reported for some decapod crustaceans (about lo-30 mg kg-‘), mainly regarding organisms from the deep sea and polar waters. There is, however, no evidence that this might be a result of antropogenic environmental contamination. Petri and Zauke (1993) hypothesised that an increased uptake of Cd might be related to general trace element deficiencies in these regions. In any case, such high Cd levels require efficient detoxification mechanisms, but, no information on this topic is available, as yet. A high interpecific heterogeneity of Cd is also apparent for copepods, covering an intermediate level, while lowest Cd concentrations are reported for euphausiids. Cu and Zn in different taxa are, despite a certain variability, well within the range found in our study (for metalbolic requirements see below). Pb is apparently low in all species under consideration. Almost no data are available for Ni and Hg in marine zooplankton. Zauke et al. (1996a) reported 2.2 + 0.5 mg Ni kg-l dry wt. (mean ~fr95% CI, N = 29) in copepods (Calanusfinmarchicus/C. helgoZandicus1from the North Sea. Unpublished data on Hg in the same copepod collectives yield 0.024 + 0.001 Hg kg-’ dry wt. (mean -t 95% CI, N = 136). While Ni in North Sea copepods is within the same range, Hg is much lower compared to values obtained for C. jinmarchicus in the present study (Table 4). As mentioned before, some elevated Ni levels have been found in C. hyperboreus and Metridia longa from the Greenland Sea (Table 4). Unpublished data suggest

268

J. Ritterhofi

G.-P. Zauke

/The

Science of tfze Total Enuironment

likewise enhanced Ni concentrations in M. Zongu from the North Sea (about 35 mg Ni kg-‘). Since no information is available on metal requirements of the zooplankton species considered in this study we will provide some tentative hypotheses relying on data from other taxa. Theoretical requirements calculated for decapod crustaceans yield 7-15 mg kg-’ dry wt. total body Cu due to enzymatic and about 25 mg kg-’ dry wt. total body Cu due to haemocyanin copper (White and Rainbow, 1985; Depledge and Bjerregaard, 1989; Rainbow, 1993). Most of the data compiled in Table 7 suggests that Cu requirements are eventually met, if requirements of the organisms considered are similar to those of decapods (which has to been proven in future studies). Only results on copepods suggest some copper deficiency. It is important to note, however, that copepods and hyperiid amphipods most probably do not posses haemocyanin (Gruner et al., 1993; Spicer and Morritt, 1995; Ritterhoff and Zauke, unpublished data on metal binding proteins). Zn concentrations in all zooplankton species compiled in Table 7 are far in excess of the theoretical enzymatic requirements calculated for decapods (20 mg kg-i dry wt., White and Rainbow, 1985; Rainbow, 1993). 4. Conclusions

Our study does not indicate generally enhanced metal availabilities for zooplankton collectives from the Fram Strait and the Greenland Sea. Rather, we are confronted with an enormous interspecific variability for which concise explanations are not at hand, as yet. In particular, high Cd concentrations in hyperiid amphipods and decapods, high Ni concentrations in the ostracod Conchoecia borealis, relatively high Hg concentrations in calanoid copepods and a substantial seasonal variation of Cd in calanoid copepods (inferred from a comparison of our data to those of Pohl, 1992) merit further investigations. Available information suggests, however, that enhanced metal levels in some organisms does not necessarily imply anthropogenic contamination. More information on the toxicokinetics especially of Ni and Hg in zooplankton organisms and on comparative uptake and depuration of all metals investi-

I99 (1997) 255-270

gated (from soluble phase and from food) during the summer time is required before a full assessment of metals in Arctic marine waters will be possible, for example, within the scope of AMAP. Acknowledgements

We thank the captain and the crew of RV ‘Polarstern’ for their kind co-operation as well as the participating scientists, especially, J. Meincke, W. Hagen and M. Rhein. Our colleague J. Frerichs helped us immensely in sampling and sorting the organisms. H.-J. Hirche kindly provided the possibility to take part in the cruise. Travel to Longyearbyen was funded by the Minister of Science and Culture of Lower Saxony and the University of Oldenburg; the analytical work was supported by the Minister for the Environment, Nature Conservation and Nuclear Safety of the Federal Republic of Germany, Umweltbundesamt (Grant: 102 04 274 to G.-P. Zauke). This study is part of the Ph.D. thesis of J. Ritterhoff, being supported by a fellowship of ‘Evangelisches Studienwerk’, D-58239 Schwerte, Germany. References Alexander, V. (1995) The influence of the structure and function of the marine food web on the dynamics of contaminants in Arctic Ocean ecosystems. Sci. Total Environ, 161, 5933603. AMAP (1995) Guidelines for the AMAP AssessmentArctic Monitoring and Assessment Programme, Oslo, Report, 95: 1. Barrie, L.A., Gregor, D., Hargrave, B., Lake, R., Muir, D., Shearer, R., Tracey, B. and Bidleman, T. (1992) Arctic contaminants: sources, occurrence and pathways. Sci. Total Environ. 122, l-74. Biittner, J.R., Borth, R., Boutwell, H.J. Broughton, P.M.G. and Bowyer, R.C. (1980) Approved recommendation (1978) on quality control in clinical chemistry. J. Clin. Chem. Clin. Biochem. 18, 78-88. Chace, F.A. (1986) Oplophoridae, nematocarcinidae. Smithson. Contr. Zool. 432, l-82. Clarke, A. and Peck, L.S. (1991) The physiology of polar marine zooplankton. Polar Res. 10, 355-369. Coachman, L.K. and Aagaard, K. (1974) Physical oceanography of the Arctic and Sub-Arctic seas. In: Y. Hermann (editor), Marine Geology and Oceanography of the Arctic Ocean. Springer, New York, pp. l-72. Depledge, M.H. and Bjerregaard, P. (1989) Haemolymph protein composition and copper levels in decapod crustaceans. Helgol. Meeresunters. 43, 207-223.

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and macrozooplankton distribution and production of dominant herbivorous copepods during spring. Polar Biol. 14, 491-503. Hurlbert, S.H. (1984) Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187-211. Hurlbert, S.H. and White, M.D. (1993) Experiments with freshwater invertebrate zooplanktivores: quality of statistical analyses. Bull. Mar. Sci. 53, 128-153. Kvambekk, A.S. and Vinje, T. (1993) The Ice Transport Through Fram Strait. Nansen Centennial Symposium, Bergen, Norway, 21-25 June. Leatherland, T.M.. Burton, J.D., Culkin, F., McCartney, M.J. and Morris, R.J. (1973) Concentrations of some trace metals in pelagic organisms and of mercury in Northeast Atlantic Ocean water. Deep-Sea Res. 20, 679-685. Locamini, S.J.P. and Presley, B.J. (1995) Trace element concentrations in Antarctic krill, Euphausia superba. Polar Biol. 15, 283-288. Macdonald, R.W. and Bewers, J.M. (1996) Contaminants in the arctic marine environment: priorities for protection. ICES J. Mar. Sci. 53, 537-563. Macdonald, C.R. and Sprague, J.B. (1988) Cadmium in marine invertebrates and arctic cod in the Canadian Arctic. Distribution and ecological implications. Mar. Ecol. Prog. Ser. 47, 17-30. Martens, S.N. and Boyd, R.S. (1994) The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 98, 379-384. Matis, J.H., Miller, T.H. and Allen, D.M. (1991) Stochastic models of bioaccumulation. In: M.C.M. Newman and A.W. Mcintosh (editors), Metal Ecotoxicology ~ Concepts and Applications. Lewis Publishers, Chelsea, USA, pp. 171-206. Nilssen, K.T., Haug, T., Potelov, V., Stasenkov, V.A. and Timoshenko, Y.K. (1995a) Food habits of harp seals (Phoca groenlundica) during lactation and moult in March-May in the southern Barents Sea and White Sea. ICES J. Mar. Sci. 52, 33341. Nilssen, K.T., Haug, T., Potelov, V. and Timoshenko, Y.K. (1995b) Feeding habits of harp seals (Phoca groenlandica) during early summer and autumn in the northern Barents Sea. Polar Biol. 15, 485-493. Oresland, V. (1995) Winter population structure and feeding of the chaetognath Eukrohnia hamata and the copepod Euchaeta antarctica in Gerlache Strait, Antarctic Peninsula. Mar. Ecol. Prog. Ser. 119, 77-86. Pacyna, J.M. (i995) The origin of Arctic air pollutants: lessons learned and future research. Sci. Total Environ. 161,39-53. PAME (1996) Working Group on the Protection of the Arctic Marine Environment. Report to the Third Ministerial Conference on the Protection of the Arctic Environment, Norwegian Ministry of Environment, Oslo, 1996. Paul, A.J., Coyle, K.O. and Ziemann, D.A. (1990) Timing of spawning of ThySanoessa raschii (Euhausiacea) and occurrence of their feeding-stage larvae in an Alaskan bay. J. Crustacean Biol. 10, 69-78. Percy, J.A. (1993) Reproduction and growth of the Arctic hyperiid amphipod Themisto libellula Mandt. Polar Biol. 13, 131-139.

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