Comparison of contaminants from different trophic levels and ecosystems

The Science of the Total Environment 245 Ž2000. 221]231

Comparison of contaminants from different trophic levels and ecosystems R. Dietz a,U , F. Riget a , M. Cleemann b, A. Aarkrog c , P. Johansen a , J.C. Hansen c a

Department of Arctic En¨ ironment, Ministry of En¨ ironment and Energy, National En¨ ironmental Research Institute, Tagens¨ ej 135, 4 floor, DK-2200 Copenhagen N, Denmark b Department of En¨ ironmental Chemistry, Ministry of En¨ ironment and Energy, National En¨ ironmental Research Institute, Frederiksborg¨ ej 399, DK-4000 Roskilde, Denmark c Risø National Laboratory, Frederiksborg¨ ej 399, DK-4000 Roskilde, Denmark Received 8 July 1999; accepted 11 July 1999

Abstract The present paper provides an overview of the priority contaminants and media from the Greenland part of the Arctic Monitoring and Assessment Program. Levels and accumulation patterns of heavy metals, POPs and a radionuclide Ž 137Cs. are compared from the terrestrial, freshwater and marine ecosystems. Of the nine compounds presented, seven ŽCd, Hg, Se, SPCB, SDDT, SHCH, HCB. increased in concentration towards higher trophic levels. For these contaminants the concentrations in soil and aquatic sediment were in the same order of magnitude, whereas the concentrations in marine biota were higher than found in the freshwater and terrestrial ecosystems probably due to the presence of longer food chains. Pb and 137Cs showed the reverse pattern compared with the other compounds. The concentrations in soil and aquatic sediments decreased in the order terrestrial, freshwater and marine ecosystems, which was reflected in the biota as well. Reindeer had similar or lower levels of Pb and 137Cs than lichens. Levels of Pb and 137Cs in marine biota did not show the same clear increase towards higher trophic as found for the other analysed compounds. Greenland Inuit contains considerably less mercury but higher levels of SPCB, SDDT and HCB than other Arctic marine top consumers. Q 2000 Elsevier Science B.V. All rights reserved. Keywords: Contaminants; Trophic comparison; Ecosystem comparison; Bioaccumulation; Greenland

U

Corresponding author. Tel.: q45-35-821415; fax: q45-35-821420. E-mail address: [email protected] ŽR. Dietz. 0048-9697r00r$ - see front matter Q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 9 9 . 0 0 4 4 7 - 7

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1. Introduction In 1993 the eight Arctic countries agreed upon the common AMAP ŽArctic Monitoring and Assessment Programme. programme ŽAMAP 1993., of which the priority Žessential . core programme was conducted for the Greenland part of the Arctic. The programme provided the opportunity to compare contaminant Žheavy metals, persistent organic pollutants or radioactivity. levels and accumulation in the same material from the terrestrial, freshwater and marine ecosystems, sampled in the same regions from the same period. Contaminants are often dealt with in a rather specialised manner. Most studies cover one contaminant group, within only one ecosystem or even just in a few or a single species. Similarly, review articles usually concentrate on one of the contaminant groups in one of the ecosystems, without providing comparisons between contaminants and ecosystems. The present overview paper is an attempt to provide such a comparison based on a graphic presentation of data. In the AMAP programme, the media for monitoring contaminant concentrations were selected from different trophic levels in the three ecosystems in order to provide information on trophic and geographical trends. In addition, the decision to implement a uniform core programme provides the basis for future monitoring of temporal trends. Not all contaminants were analysed in all sampled media Žsee Table 1., but a number of comparisons and conclusions could be drawn based on the available data. Additional information is available from previous investigations on other matrices, species and contaminants in Greenland, especially with respect to heavy metals and radioactivity Že.g. Dietz et al., 1996; Aarkrog et al., 2000.. A review of the data from the whole Arctic have been carried out as part of the AMAP assessment for all three contaminant groups separately, and is not included in this review ŽdeMarch et al., 1998; Dietz et al., 1998; Strand et al., 1998..

2. Materials and methods Data from the 1994 and 1995 Greenlandic study

were extracted from the DanishrGreenlandic part of the AMAP programme, as presented in the National Assessment report, together with the few data available regarding contaminants in human tissue ŽHansen et al., 1995; Mulvad et al., 1996; Aarkrog et al., 1997.. The basic data used in this presentation are geometric mean values; each value is derived from up to 25 measurements from one to four geographic areas in Greenland. The number of samples analysed therefore was relatively large: approximately 850 for heavy metals, 500 for POPs, and 100 for radionuclides. Not all available data were selected for interpretations contained here Žsee Selection of data and Table 1 below.. The advantage with the DanishrGreenlandic AMAP selection was that heavy metals, POPs and radionuclides were analysed in the same animals, representing the same geographical regions and sampled over the same period of time from the terrestrial, the freshwater and the marine ecosystems. Details of material and methods, data and statistical handling of the data are not dealt with in detail, as they are presented elsewhere in this issue ŽAarkrog et al., 2000; Aastrup et al., 2000; Cleemann et al., 2000a,b,c; Riget and Dietz, 2000; Riget et al., 2000a,b,c,d..

3. Selection of data Contaminants were analysed in the following compartments: whole samples Žsediment, soil, humus, lichen, Centraria ni¨ ialis and moss, Rhacomitium lanuginosum., soft parts Žblue mussel, Mytilus edulis., or in liver for most of the other species. Exceptions were POPs in ringed seal Ž Phoca hispida. and humans Ž Homo sapiens. where blubber and adipose tissue was analysed and 137 Cs was analysed in muscle tissue in shorthorn sculpin Ž Myoxocephalus scorpius., glaucous gull Ž Larus hyperboreus. and ringed seal. In most cases the AMAP programme prescribe tissues where contaminant concentrations are known to be highest, e.g. mercury in liver and POPs in blubber Žsee Table 1.. Soil, sediment, and vegetation results are reported as mgrg for metals and POPs and as Bqrkg for 137 Cs, all on dry weight Ždry wt.. basis, because the water content in these samples is

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223

Table 1 Summary of media, selected subsamples, number Ž N . of samples from each major sample area in Greenland, and the reporting format of the analysis used in the graphic comparisona Ecosystem

Media

Pb

Cd

Hg

Se

POPs

Cs-137

Terrestrial

Soil

0]15 cm Ž5r5r5r5.

0]15 cm Ž5r5r5r5.

0]15 cm Ž5r5r5r5.

] ]

] ]

0]15 cm Ž3r3r3r3.

Humus

Ž5r5r5r5.

Ž5r5r5r5.

Ž5r5r5r5.

Ž5r5r5r5.

]

]

Lichen Ž Centraria ni¨ ialis . Moss Ž Rhacomitium lanuginosum. Reindeer

Ž5r5r5r5. dw

Ž5r5r5r5. dw

Ž5r5r5r5. dw

Ž5r5r5r5. dw

]

Ž3r3r3r3. ww

Ž5r5r5r5. dw

Ž5r5r5r5. dw

Ž5r5r5r5. dw

Ž5r5r5r5. dw

]

]

3.1 years Ž6r7. liver ww

3.1 years Ž6r7. liver ww

3.1 years Ž6r7. liver ww

3.1 years Ž6r7. liver ww

]

3.1 years Ž6r8. muscle ww

Sediment

0]1 cm Ž5r5r5r5. dw ]

0]1 cm Ž5r5r5r5. dw ]

0]1 cm Ž5r5r5r5. dw 35.9 cm Ž23r21r21r50. muscle ww

]

0]1 cm Ž1r1r1r1. dw 26]136 cm Ž25r25r25r25. muscle ww

0]10 cm Ž3r3r3r3. ww

]

0]1 cm Ž5r5r5r5. dw Lipid norm. Ž14r15r15. so.tis.ww ]

0]3 cm Ž1r1r1r1. dw All Ž3r1r1. so.tis.ww ]

Femalesb Ž15r15r13r17.

All Ž3r3r3r3.

Freshwater

Arctic Char

Marine

Sediment

Blue mussel

Polar cod

Shorten sculpin

Iceland gull

Glaucous gull

Ringed seal

Human a

Ž3r3r5r4. muscle ww

0]1 cm Ž5r5r5r5. Li norm.dw 5.2 cm Ž14r15r15. so.tis.ww All Ž24r25. liver ww 24.3 cm Ž25r25r 25r25. liver ww All Ž6r8. liver ww All Ž25r19r 17r22. liver ww G 7 years Ž7r2r5. liver ww

0]1 cm Ž5r5r5r5. Li norm.dw 5.2 cm Ž14r15r15r. so.tis.ww All Ž24r25. liver ww All Ž25r25r 25r25. liver ww 2C & 3C Ž12r6. liver ww Adult Ž6r12r3r22.

0]1 cm Ž5r5r5r5. Li norm.dw 5.2 cm Ž14r15r15. so.tis.ww 23 cm Ž24r25. liver ww 24.3 cm Ž25r25r 25r25. liver ww All Ž6r8. liver ww All Ž25r19r17r22.

5.2 cm Ž14r15r15. so.tis.ww All Ž24r25. liver ww 24.3 cm Ž25r25r 25r25. liver ww 2C & 3C Ž12r6. liver ww Adult Ž6r12r3r22.

liver ww ]

muscle ww ]

Adults Ž6r12r3r22.

All Ž3r3r3r3.

liver ww G 7 years Ž7r2r5. liver ww

liver ww G 7 years Ž7r2r5. liver ww

liver ww G 7 years Ž7r2r5. liver ww

liver ww G 7 years Ž7r2r5. blubber ww

muscle ww All Ž3r3r3r3. muscle ww

]

]

Ž18. liver ww

]

Ž42. adi.tis.ww

]

Abbreviations used are ww, wet weight; dw, dry weight; so.tis., soft tissue; adi.tis., adipose tissue; Li norm, lithium normalised. Lipid normalised.

b

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very variable and cannot be expressed on a wet weight basis in a well defined way. Animal tissue results are also presented as mgrg for metals and POPs and as Bqrkg for 137 Cs, but on a wet weight Žwet wt.. basis. Data are presented in this way in the other papers of this special issue. The scientific literature normally also deals with data on a fresh weight basis, since this is the most representative for the food intake. For visceral tissues the dry weight concentrations are typically 3]5 times higher than the wet weight concentrations, but in tissues with a low water content Že.g. blubber ., the differences are minor. The data presented in this overview is not ideal for comparative purposes. Species from more directly linked food chains, the same tissue or matrices, the same weight basis as well as more uniform season, area, age, sex would have been ideal for the comparisons. However, as the primary gold in this paper is to compare the relative accumulation pattern among contaminants from the programme, and as all contaminants are treated in a similar manner, the overview still shows some useful patterns. A graphics logarithmic form of presentation was chosen and no bioaccumulation factors were calculated due to

the limitation of the comparability of the data. In addition most comparisons and conclusions are drawn among comparable matrices. An overview on the basic information of the samples used in the comparisons are presented in Table 1.

4. Results and discussion 4.1. Lead The highest lead levels are found in soil Žterrestrial ecosystem. and aquatic sediments Žfreshwater and marine ecosystems.. The levels are quite similar even though they represent three different ecosystems ŽFig. 1.. Lead levels in humus representing organic material are 2]3 times lower than in soil. Lead does not accumulate towards higher trophic levels in the terrestrial or the marine ecosystem. Lead levels in reindeer livers are lower than in lichens. Lichens again, have lower lead levels than in moss and humus. In the marine ecosystem, blue mussels have the highest lead levels among biota. Lead levels in shorthorn sculpin and polar cod Ž Boreogadus saida., Iceland gull Ž Larus glau-

Fig. 1. Summary of the ranges of lead means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

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coides., glaucous gull and seals analysed are very low Žlower than or close to the detection limit.. In terms of biota samples, lead levels in the terrestrial ecosystem are higher than in the marine ecosystem. 4.2. Cadmium Unlike lead, cadmium levels increase towards higher trophic levels in both the terrestrial and the marine ecosystem ŽFig. 2.. Although marine and freshwater sediments show similar cadmium levels, the cadmium levels in the marine ecosystem are higher than in the terrestrial ecosystem. Being a herbivore, reindeer have cadmium levels in the liver that are approximately 50 times lower than in ringed seals which are a fourth to fifth trophic level consumer ŽHobson and Welch, 1992.. Within the marine ecosystem, adult ringed seals are highest and glaucous gulls have the second highest cadmium levels. Polar cod and Iceland gulls have the lowest cadmium levels. Biomagnification of cadmium within the Arctic marine ecosystem is dependant on the species compared, which has been documented by a number of authors. Muir et al. Ž1992, 1997. provide increas-

225

ing biomagnification factors for cadmium in waterralgae Ž2.4 = 10 5 ., fishrseal Ž10.5., fish rnarwhal Ž80. from the eastern Canadian Arctic marine food chain. However, examples of a lack of increases are also provided from, e.g. algaercopepod Ž1.1., amphipodrfish Ž0.04. and sealrbear Ž0.4.. Based on a review of as many as 5000 samples Dietz et al. Ž1996. describe the Greenlandic ecosystem with comparison of various tissues. As for the Canadian survey examples of both increases and decreases can be found dependant of the compared species. Further discussion on bioaccumulation from the whole Arctic is provided in Dietz et al. Ž1998.. 4.3. Mercury Like cadmium, mercury levels increase towards higher trophic levels, but biomagnification is slightly greater ŽFig. 3.. The mercury levels in soil, freshwater sediments and marine sediments are quite similar. Mercury levels in humus cover the concentration range observed in soil, lichen and moss, all of which may be part of humus. Blue mussels and fish have lower concentrations than humus, lichens and moss a difference that would

Fig. 2. Summary of the ranges of cadmium means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

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Fig. 3. Summary of the ranges of mercury means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

be reduced if the marine samples were presented on a dry weight basis. Gulls and seals, on the other hand, have higher mercury levels than terrestrial plants and reindeer. The higher concen-

trations found in the gulls and seals may be attributed to their trophic position as a fourth to fifth trophic level consumer ŽHobson and Welch 1992.. Biomagnification of mercury within the

Fig. 4. Summary of the ranges of selenium means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

R. Dietz et al. r The Science of the Total En¨ ironment 245 (2000) 221]231

Arctic marine ecosystem has been documented by a number of authors. Muir et al. Ž1992, 1997. provide increasing biomagnification factors for mercury in fishrseal Ž163., fishrnarwhal Ž305. and sealrbear Ž12.3. from the eastern Canadian Arctic marine food chain. Dietz et al. Ž1996, 1998. provide ecosystem with comparisons to a large number of tissue related biomagnification factors including crustacean, mollusc, bird seal and whale species from Greenland waters ranging from 1.8 to 2823. Only one case fails to show a biomagnification, namely when levels in ringed seal muscle are compared to polar bears ŽUrsus maritimus.. In general the mercury biomagnification factors were larger than the comparable factors for cadmium. Mercury concentrations in human liver tissue are more than a factor of 10 lower than in ringed seals. This is likely to be related to the fact that human samples were obtained from the Nuuk area, a region where a considerable amount of imported food is ingested. The mercury levels in human blood are clearly correlated to the proportion of marine game consumed, as demonstrated by several authors Že.g. Hansen, 1990; Hansen et al., 1998.. Nuuk hunters have less than 20% of the mercury concentration in the blood compared with hunters from Avanersuaq, where marine mammals comprise a larger proportion of the diet ŽHansen 1990.. 4.4. Selenium In the marine ecosystem higher selenium levels are found than in the terrestrial ecosystem. The trophic accumulation within each of the ecosystems is moderate, and much smaller than for cadmium and mercury ŽFig. 4.. No selenium data are available from soil and sediments. Blue mussels and marine fish have the lowest selenium concentrations in the marine ecosystem, similar to the highest observed concentrations observed in reindeer from the terrestrial ecosystem. 4.5. Ý PCB and Ý DDT POP analyses in the AMAP program were car-

227

ried out in fewer compartments than for the heavy metals and therefore provide less coverage of the ecosystems. ÝPCB and ÝDDT behave in a similar manner to mercury, even though the concentrations are approximately 10]100 times lower in sediments and 10 times lower in biota. The freshwater and marine sediment levels are similar, as was also found to be the case for lead, cadmium and mercury. Thus, the ÝPCB and ÝDDT input from ocean currents are not large enough to result in detectable differences between marine sediments and freshwater sediments. The lack of an ocean derived signal for ÝPCB and ÝDDT is in accordance with Macdonald and Bewers Ž1996., who stated that the primary medium for long range transport of semi-volatile and insoluble substances is the atmosphere rather than the sea. ÝPCB and ÝDDT show a similar trophic accumulative pattern as mercury, and for all three contaminant groups, the levels in ringed seals are 1000 times higher than in blue mussels, whereas cadmium and selenium levels are 100 and 10 times higher, respectively. The ÝPCB and ÝDDT levels in land-locked Arctic char and shorthorn sculpin are similar, representing the freshwater and marine media, respectively. The glaucous gull and ringed seal contain higher concentrations of ÝPCB and ÝDDT due to a higher trophic position. Trophic related increases in POP levels have been documented previously by a number of authors Že.g. Muir et al., 1988, 1992, 1997.. In contrast to mercury, ÝPCB and ÝDDT are higher Ž2]45 times. in human adipose tissue than in ringed seal blubber and glaucous gull livers, which have the highest ÝPCB and ÝDDT concentrations in the marine food chain. The high human concentrations of ÝPCB and ÝDDT in Nuuk, Greenland Ž15.8 and 4.45 mgrg, respectively. are among the highest levels observed in the Arctic ŽMulvad et al., 1996; Hansen et al., 1998.. It is very surprising that the levels are so high, since polar bears, which feed mainly on ringed seal blubber, only have ÝPCB and DDE ranging from 4.56]8.04 to 0.213]0.268 mgrg lipid wt., respectively, from the same geographical region ŽNorstrom et al., 1998..

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4.6. Ý HCH and HCB ÝHCH and HCB show a similar picture as that found for ÝPCB and ÝDDT. ÝHCH levels in freshwater sediments are similar to those in marine sediments This could not be evaluated for HCB, as HCB was not an AMAP priority contaminant in marine sediment. The levels of HCB in ringed seal are 100 times higher than in blue mussels, reflecting a weaker biomagnification compared with ÝPCB and ÝDDT. It is noteworthy that HCB levels in ringed seals were lower than in glaucous gulls. The weaker bioaccumulation of ÝHCH and HCB relative to ÝPCB and ÝDDT is consistent with differences in the water solubility of the two groups. Compounds with low water solubility are efficiently accumulated across gills and via the gut of aquatic animals ŽMuir et al., 1997.. ÝPCB and ÝDDT have water solubilities Ž10y8 to 10y10 grl. that are two to three orders of magnitude lower than for values of ÝHCH and HCB wTanabe and Tatsukawa, 1983 cited in Muir et al. Ž1997.x. As found for the ÝPCB and ÝDDT, HCB is higher in human adipose tissue than in ringed seals and glaucous gull, which have the highest HCB concentrations in the marine food chain. 4.7.

137

137

Cs

Cs levels are highest in the terrestrial ecosystem, intermediate in the freshwater ecosystem and lowest in the marine ecosystem. This was

reflected in both the abiotic and biotic media. Reindeer had similar or lower content of 137 Cs than lichens. Sediment levels were 20]100 times higher than water concentrations, which in turn were similar to the levels found in blue mussels. A weak increase towards higher trophic levels was observed in the marine biota, but only by a factor of 10 from the lowest to the highest concentrations.

5. Overall discussion As seen from Figs. 1]9, of the nine presented compounds, seven ŽCd, Hg, Se, ÝPCB, ÝDDT, ÝHCH, HCB. showed an increase towards higher trophic levels. For these contaminants, concentrations were in the same order of magnitude in soil and aquatic sediment although some geographical differences were observed. In marine biota, however, concentrations generally were higher than in terrestrial and freshwater biota. This may be explained by the longer food chains in the marine ecosystem combined with the observed biomagnification. This general pattern is similar to most other parts of the Arctic ŽMuir et al., 1997., although certain areas may differ from this. Cadmium levels in terrestrial birds and mammals such as caribou, moose and ptarmigan are very high in the Yukon area in the western Canadian Arctic. This has been attributed to the local geology ŽDietz et al., 1998.. In this area caribou, for example, can have up to 10 times higher cadmium

Fig. 5. Summary of the ranges of ÝPCB means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

R. Dietz et al. r The Science of the Total En¨ ironment 245 (2000) 221]231

levels in liver than the Greenland reindeer, and most marine mammals species from this area have cadmium levels that are 2]6 times lower than in Greenland ŽIbid.. For lead and 137C the pattern observed was the

229

reverse of that for the other compounds presented. The concentrations in soil and aquatic sediments decreased in the order: terrestrial, freshwater and marine ecosystem. This was reflected in the biota as well. Reindeer had similar

Fig. 6. Summary of the ranges of ÝDDT means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

Fig. 7. Summary of the ranges of ÝHCH means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

Fig. 8. Summary of the ranges of HCB means Žgeometric. in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

230

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Fig. 9. Summary of the ranges of 137 Cs means Žarithmetic . in Greenland terrestrial, freshwater and marine AMAP medias. For information on normalisation, number Ž N ., matrix and weight basis see Table 1.

or lower levels of lead and 137 Cs than lichens. Levels of Pb and 137Cs in marine biota did not show the same clear increase towards higher trophic as found for the other analysed compounds. In the scientific literature recent reviews provide further information on Arctic ecosystems. The general pattern found in the present overview is supported by data for other species Že.g. deMarch et al., 1998; Dietz et al., 1998; Strand et al., 1998.. The majority of food consumed by the local Greenland population originates from the marine ecosystem ŽT. Pars, pers. comm... Thus, the Greenland population will be particularly exposed to cadmium, mercury and POPs, whereas the exposure to lead and radionuclides will be low. The high exposure is reinforced by the fact, that in several Greenland municipalities, seabirds, seals, whales, and polar bears still constitute a substantial part of the diet. Studies of the Greenland Inuit population confirm that local food is the most important source of mercury and POPs, as some of the highest mercury and POP levels in the Arctic and in the

World are found in the Greenland Inuit Že.g. Mulvad et al., 1996; Hansen et al., 1998.. Acknowledgements We wish to thank The Danish Environmental Protection Agency, who provided the funding for the Danish part of the AMAP program constituting the basic data for this overview article. M. White, Danbiu ApS improved the linguistics and three anonymous referees improved the manuscript. References Aarkrog A, Aastrup P, Asmund G et al. AMAP Greenland 1994]1996. Arctic Monitoring and Assessment Programme. Danish Environmental Protection Agency, Environmental Project No. 356: 1997:788. Aarkrog A, Dahlgaard H, Nielsen SP. Environmental radioactive contamination in Greenland: A 35 years retrospect. Sci Total Environ 2000;245:233]248. Aastrup P, Riget F, Dietz R, Asmund G. Zinc, cadmium, mercury, selenium and copper in Greenland caribou. Sci Total Environ 2000;245:149]160. AMAP. The monitoring programme for Arctic Monitoring and Assessment Programme. Oslo, Norway: AMAP, 1993.

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