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Bioaccumulation of radiocaesium in Arctic seals from Northeast Greenland JoLynn Carrolla,* , Kristina Rissanenb , Tore Haugc a Akvaplan-niva, Polar Environmental Centre, Tromsø, Norway b URadiation and Nuclear Safety Authority, Helsinki, Finland c Institute of Marine Research, Tromsø, Norway
Abstract Seals are high trophic level feeders that bioaccumulate many contaminants to a greater degree than most lower trophic level organisms. Their trophic status in the marine food web and wide-spread distribution make seals useful sentinels of arctic environmental change. In 1999 and 2000 seals were captured from the northeast coast of Greenland (75– 80◦ N) in order to document the levels and bioaccumulation potential of radiocaesium in the high latitude seal species: harp, ringed, and hooded seals. The results are compared with previous studies in order to assess geographic differences in bioaccumulation for Arctic seals. Concentrations of 137 Cs were determined in muscle, liver and kidney samples from a total of 25 juvenile and 3 adult seals. The mean concentration in muscle and liver samples for all animals was 0.36 ± 0.14 Bq/kg f.w. and 0.26 ± 0.08 Bq/kg f.w. The results are consistent with previous studies indicating low levels of radiocaesium in Arctic seals in response to a long term trend of decreasing levels of 137 Cs in the Greenland Sea region. Comparing levels in muscle tissue among the different seal species, the 137 Cs activity concentration of harp (0.36 ± 0.14 Bq/kg f.w.) and hooded seals (0.37 ± 0.14 Bq/kg f.w.) are similar within uncertainty limits while average concentrations in ringed seals are slightly lower (0.2 Bq/kg f.w.). Bioconcentration factors (BCFs) for the seals (30–110) correspond well with the variety of prey consumed by seals in this region indicating that diet selection is a dominant factor controlling bioaccumulation of radiocaesium in these Arctic seals. Keywords: Bioaccumulation, Radiocaesium, Seals, Greenland
1. Introduction Seals are among the most quantitatively important mammals in the upper part of the marine food chain, along with whales, walrus and polar bear (WWF, 2004). Due to the importance of seals in subsistence diets of Arctic indigenous peoples, they are a major focus of several on-going monitoring and protection efforts (AMAP, 2002). The results of this investigation provide critical information on concentrations of the radionuclide 137 Cs (radiocaesium) which is among the more pervasive elements found in the Arctic. * Corresponding author. Address: Akvaplan-niva AS, Polar Environmental Centre, Tromsø, phone: (+47) 7775 0314 +; fax: (+47) 7775 0301 +; e-mail: [email protected]
RADIOACTIVITY IN THE ENVIRONMENT VOLUME 8 ISSN 1569-4860/DOI 10.1016/S1569-4860(05)08018-6
© 2006 Elsevier Ltd. All rights reserved.
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The main sources of radiocaesium to the Arctic are discharges from Europe’s nuclear reprocessing facilities. It is estimated that these facilities have contributed 10–15 PBq to the Arctic Ocean as compared to global fallout and Chernobyl which have contributed 4.1 PBq and 1–5 PBq, respectively (Aarkrog, 1994; Strand et al., 1997). Discharges from Sellefield (UK) and La Hague (France), the two largest reprocessing facilities, enter the Irish Sea and English Channel, respectively. After mixing with Chernobyl-laden water from the Baltic Sea in the North Sea, the plume of radiocaesium is transferred further northward by the Norwegian Coastal Current. Once in the Norwegian Sea, the caesium-laden current bifurcates with one branch leading into the Barents Sea (Barents Sea Overflow Current) and the other branch (West Spitzbergen Current) traversing around the west coast of Svalbard (Kershaw and Baxter, 1995; Kershaw et al., 1997; Heldal et al., 2003) (Fig. 1). Part of the northward flowing West Spitzbergen Current detaches and is re-circulated within the Greenland Sea. The transport time for radiocaesium from the North Sea into the Greenland Sea has been estimated to be on the order of 5 years (Dahlgaard, 1995). This caesium enriched water further mixes with lower concentration Arctic Ocean water entering the North Atlantic via the Fram Strait. A number of regional sources of radionuclides exist in the adjacent Norwegian, Barents, and Kara Seas. These secondary sources of radioactive contamination to northern European waters include fluvial inputs from nuclear facilities on the Ob and Yenisey Rivers, point source inputs from radioactive waste dump sites and nuclear test sites on the Russian coastline. Included as well are the nuclear operations related to the military-industrial complex in the Kola Peninsula. Several nuclear accidents have occurred in the region (AMAP, 1998; Matishov et al., 2002) and on-going activities in the region have been identified as possibili-
Fig. 1. Generalized pathway of radiocaesium transport from Sellefield (UK) and La Hague (France) into the Arctic Ocean. In Greenland waters, radiocaesium from Sellefield is returning from the Arctic Ocean. Seal bioconcentration factors (BCF) among different sub-regions of the European Arctic are also shown.
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ties of accidents in the future (Strand et al., 1997). Of greatest concern are the Kola nuclear power plant reactors, nuclear submarines or icebreakers, waste disposal, nuclear weapons or military activities in Murmansk and Archangelsk regions, Novaya Zemlya installations, and military-industrial sites located within catchment areas of the rivers Ob and Yenisey. Levels of radioceasium around northeast Greenland began declining in the mid-1970s in response to a decline in discharges from Sellefield four years earlier (Matishov and Matishov, 2004). During the early to mid-1970s surface seawater concentrations in the Greenland Sea above 65◦ N were on the order of 9 Bq/m3 . In the early to mid-1990s, concentrations had decreased to approximately 7 Bq/m3 (Aarkrog et al., 2000). Among the wide variety of radionuclides present in the Arctic environment, radiocaesium is the only radionuclide that has been shown to biomagnify through marine food webs (Calmet et al., 1992; Kasamatsu and Ishikawa, 1997; Watson et al., 1999; Heldal et al., 2003; Zhao et al., 2001). And it has been hypothesized that features unique to Arctic ecosystems lead to increased vulnerability for organisms from contaminant releases (Fisher et al., 1999; Carroll and Carroll, 2003). These features include: the seasonal and spatial focus of primary productivity, strong benthic-pelagic coupling, a prevalence of large mammals as apex predators, and relatively large amplitude fluctuations in the lipid cycle of some species. Few studies have been conducted on Arctic marine mammals and in particular for seals (Aarkrog et al., 2000; Rissanen et al., 1997; Carroll et al., 2002). Better knowledge is needed of the bioaccumulation potential of apex predators for a variety of species, habitats, and environmental conditions. The present study provides an opportunity to examine the levels and bioaccumulation potential for radiocaesium in harp, ringed, and hooded seals from NE Greenland. The data are used in conjunction with previous work to compare differences among Arctic seal populations from several locations. This knowledge will lead to more effective use of seals and other marine mammals as indicators of environmental change in Arctic marine monitoring programmes.
2. Methods 2.1. Field sampling A research vessel was used to search for harp, hooded, and bearded seals along the drift ice edge areas of the east coast of Greenland in Fall 1999 and Summer 2000 (Table 1). Animals were weighed to the nearest 1/2 kg and sex and sexual maturity (juveniles and adults) were determined. Sub-samples of seal muscle, liver, and kidney were removed and frozen at −20◦ C until analyses were performed. Ages of seals were estimated by counting of growth layers on teeth extracted from individuals as described in Haug et al. (2004). Samples were analyzed at the Radiation and Nuclear Safety Authority in Finland. Muscle, liver and kidney samples from individual seals were cleaned, cut into small pieces, dried at 105◦ C and homogenized. Each sample was placed in a Marinelli beaker or in 100 or 35 ml plastic jars. Samples were counted on a high-purity, low background, gamma spectrometer for time periods ranging from 900–6800 minutes. The spectrometer was calibrated using matrixmatched standards in a similar geometry.
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Table 1 Radiocaesium concentrations (Bq/kg f.w.) in seal muscle and liver tissue. Ringed, hooded, and harp seals were captured in October 1999 from Northeast Greenland Species
Weight (kg)
Age (yrs)
Sex
Muscle (Bq/kg f.w.)
Liver (Bq/kg f.w.)
Ringed Ringed Ringed Harp Harp Harp Harp Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded
21 58 47 62 58 54 32 36 43 205 36 39 43 56 35 45 32 27 38 41 34 66
<1 10 >20 1 2 1 <1 <1 <1 10 <1 <1 <1 <1 <1 <1 <1 <1 <1 <1 <1 1
M M M M M M M F F M M M M M M F F M M M F M
<0.2 0.2 ± 0.05 <0.2 0.39 ± 0.04 0.29 ± 0.06 0.30 ± 0.06 0.44 ± 0.05 0.25 ± 0.05 0.36 ± 0.09 0.44 ± 0.08 0.26 ± 0.07 0.45 ± 0.07 0.32 ± 0.05 0.72 ± 0.13 0.18 ± 0.04 <0.4 <0.2 <0.5 <0.3 0.37 ± 0.05 0.24 ± 0.04 0.40 ± 0.07
0.18 ± 0.03 0.32 ± 0.07 – 0.21 ± 0.05 <0.30 <0.13 0.36 ± 0.05 <0.17 0.32 ± 0.07 0.20 ± 0.04 0.16 ± 0.03 0.36 ± 0.06 0.24 ± 0.05 – <0.10 <0.20 – – – 0.20 ± 0.04 <0.24 –
Mean ± stdev Ringed
0.20 n=3
Mean ± stdev
0.36 ± 0.07
Harp Mean ± stdev
n=4 0.37 ± 0.15
Hooded
n = 15
Mean ± stdev All
0.36 ± 0.13 n = 22
0.25 ± 0.07 n=2
0.25 ± 0.08 n = 10 0.26 ± 0.08 n = 16
3. Results 3.1. Radiocaesium levels Samples of muscle, liver, and kidney taken from seals collected in 1999 and 2000 were analyzed as described in the previous section and are summarized in Table 1 and Table 2 respectively. The 137 Cs activity concentration of seal muscle for all animals (1999 and 2000 combined) was relatively low (mean = 0.37 ± 0.14 Bq/kg f.w.; n = 22). 137 Cs concentrations in liver were slightly lower than in muscle (mean = 0.26 ± 0.08 Bq/kg f.w.; n = 14).
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Table 2 Radiocaesium concentrations (Bq/kg f.w.) in muscle, liver and kidney tissue from hooded seals collected from Northeast Greenland in July 2000 Species
Weight (kg)
Age (yrs)
Sex
Muscle (Bq/kg f.w.)
Liver (Bq/kg f.w.)
Kidney (Bq/kg f.w.)
Hooded Hooded Hooded Hooded Hooded Hooded
75 81 70 88 90 139
2 2 4 5 8 16
M M M F F M
0.44 ± 0.05 0.22 ± 0.04 0.23 ± 0.04 0.60 ± 0.06 0.34 ± 0.05 0.59 ± 0.06
0.34 ± 0.04 <0.1 <0.1 0.34 ± 0.05 0.17 ± 0.03 0.26 ± 0.04
0.20 ± 0.04 0.11 ± 0.04 0.16 ± 0.04 0.23 ± 0.04 0.35 ± 0.06 0.23 ± 0.04
0.40 ± 0.17
0.28 ± 0.08
0.35 ± 0.06
Mean ± stdev
Kidney samples were taken only during the 2000 expedition, and contained 137 Cs in concentrations similar to liver (mean = 0.21 ± 0.08 Bq/kg f.w.; n = 6). Comparing levels in muscle tissue among the different seal species, the 137 Cs activity concentration of harp and hooded seals are similar within uncertainty limits while ringed seals contain significantly lower radiocaesium concentrations despite similarities in animal sizes among the three species examined (Table 1). However there were no corresponding differences in 137 Cs activity concentration in liver samples among the three species examined during the investigation. 3.2. Radiocaesium bioconcentration factors Bioconcentration factors (BCFs) normalize radiocaesium tissue levels for spatial and temporal differences in environmental concentrations. The bioconcentration factor (BCF) is defined as BCF = CORG (Bq/kg fresh weight)/CSW (Bq/kg), CORG = concentration in the organism, CSW = concentration in seawater. The BCFs for NE Greenland seals were calculated taking the radiocaesium concentration measurements in individual muscle tissue samples and dividing these by a seawater concentration of 6.6 Bq/m3 . The resulting range of BCF values is from 30–110 (Table 3). This seawater concentration was estimated by extrapolating the long-term linear trend of decreasing seawater concentrations as measured in the waters surrounding NE Greenland and described by Aarkrog et al. (2000). Aarkrog et al. (2000) report that the mean seawater concentration during 1990–1997 in NE Greenland between 70–65◦ N, 75–70◦ N and 80–75◦ N were 7.1 ± 2.2, 7.1 ± 1.8 and 7.1 ± 1.3, respectively. There is little change to our determined BCF values as a result of the extrapolated decrease in seawater concentrations from the early to late 1990s. Certainly these minor differences do not alter the overall conclusions of this investigation.
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Table 3 Bioconcentration factors (BCFs) in muscle tissue of marine mammals collected from different regions of the Northern European seas Location
Marine mammal
Time period
BCF value
Source
NE Greenland NE Svalbard White Sea/Kola Peninsula Greenland Barents/Norwegian Seas Svalbard Barents Sea
Seals Seals Seals Marine mammals Harbour porpoise Minke whales Minke whales
1999–2000 2000 1994–1995 1990–1997 1998–2000 1998 1998
30–110 34–130 60 ± 20 114 165 ± 5 70–150∗ 130–285∗
Present study Carroll et al., 2002 Rissanen et al., 1997 Aarkrog et al., 2000 Heldal et al., 2003 Born et al., 2002 Born et al., 2002
∗ Calculation made assuming a seawater concentration range of 2.0–4.4 Bq/kg for 137 Cs (Heldal et al., 2003).
4. Discussion 4.1. Radiocaesium levels in seals Seals living at the ice edge in the Greenland Sea are continuously exposed to radiocaesium. Conditions of chronic low level radioactive contamination, such as are present in the Greenland Sea today, lead to food chain transfer as the dominant pathway of exposure for marine organisms (Fowler, 1982; Rowan and Rasmussen, 1994; Zhao et al., 2001). Approximately 70% of the body burden of radiocaesium accumulates in muscle tissue with the additional 30% taken up by other parts of the organism (Anderson et al., 1990). Studies of dissected seal pups from Northwest Russia indicate that radiocaesium concentrations are highest in soft tissues (e.g. parathyroid gland, pancreas, cartilaginous tissues, ovaries) and lowest in bones and fat (Rissanen et al., 1999). Since radiocaesium levels in the seas surrounding the Arctic Ocean are currently very low, seals from NE Greenland would be expected to contain correspondingly low concentrations in their tissues and organs. Concentrations are highest in NE Greenland as compared to other sections of Greenland. This is a consequence of the influence of the recirculation currents originating from the West Spitzbergen Current which contain relatively high concentrations of radiocaesium derived mainly from the European reprocessing facilities (Aarkrog et al., 2000). The overall low mean radiocaesium concentration of 0.37 ± 0.14 Bq/kg in seal muscle, confirms the expectation that regional sources in addition to the main sources (reprocessing facilities, Chernobyl, global fallout) have thus far not had a significant impact on the marine ecosystem. Radiocaesium levels have not changed since 1990–1994 (0.40 ± 0.12 Bq/kg) and are in accordance with the long-term trend of slowly diminishing radiocaesium concentrations in seawater since 1970 (Aarkrog et al., 2000; Aarkrog, 1997a, 1997b). Concentrations in NE Greenland seals are slightly higher as compared to concentrations in seal pups taken from NE Svalbard during the same year (Spring 1999). In NE Svalbard the mean concentration for all animals was 0.23 ± 0.04 Bq/kg f.w. (n = 11) (Carroll et al., 2002). These differences mirror the higher radiocaesium concentrations detected in seawater from NE Greenland (∼6.6 Bq/m3 ) as compared to NE Svalbard (2.0–4.7 Bq/m3 ) and are
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a consequence of the greater influence of Europe’s nuclear reprocessing facilities on the waters surrounding Greenland as compared to Svalbard. 4.2. Radiocaesium bioconcentration in seals The bioaccumulation of radiocaesium in seals represents the outcome of many factors involving a combination of physiological factors, such as absorption efficiency, and ecological factors including diet selection, feeding rates, and prey availability. Migration patterns will also determine the amount of radiocaesium accumulated from food and subsequently retained in the body due to variations in seawater concentrations along the main transport pathway to the Arctic from the main source areas (Fig. 1). Comparing different regions of the Arctic, seals have the lowest BCF values, followed by porpoises, while whales generally have the highest BCF values (Table 3). The BCFs reported for seals from NE Greenland and NE Svalbard further agree well with the value reported previously by Aarkrog et al. (2000) for marine mammals from all of Greenland’s coastal waters (BCF = 114) indicating that these various data sets provide a consistent picture of radiocaesium biouptake in Arctic seals. Among the wide variety of radionuclides present in the Arctic environment, radiocaesium can biomagnify through marine food chains (Anderson et al., 1990; Kasamatsu and Ishikawa, 1997; Fisk et al., 2001; Zhao et al., 2001). Biomagnification of radiocaesium implies that the trophic status of primary prey items is an important factor affecting the radiocaesium activity concentration of seals. As a result, a clear effect of diet selection on radiocaesium bioaccumulation would be expected. BCFs reported for prey items from the Barents and Norwegian Seas (Heldal et al., 2003) and in the waters surrounding Greenland (Aarkrog et al., 2000) for omnivorous fish, benthic organisms, and carnivorous fish are within an approximate range of 10–100. Thus the relatively low BCF values obtained for seals from the European Arctic indicate only a slight enhancement of radiocaesium in relation to prey species (Table 3). Given that life-times of seals (∼30 years) are significantly longer than for prey species (∼5–15 years) we would expect that over time, seals would bioaccumulate increasingly high levels of radiocaesium resulting in correspondingly higher BCF values. While this is apparently not the case for Arctic seals, studies of other marine mammals report a clear increase in bioaccumulation relative to potential lower trophic level prey items, for example, Harbour porpoises (BCF = 165 ± 5) and Minke whales (BCF = 130–285) from the Barents Sea (Table 3). Yet these findings are in contrast to those of Aarkrog et al. (2000) who report no significant differences in radiocaesium contamination between whales and seals taken from Greenland waters. The resulting low BCF values for seals from NE Greenland may be related to the relatively young age of seals in the present study in combination with diet selection factors. The BCF value would be expected to be relatively low if the diet selection of seals consists of organisms relatively low on the trophic pyramid. Analyses of stomach and intestinal contents from hooded and harp seals captured in the pack ice belt of the Greenland Sea in summer (July–August) of 2000 and winter (February–March) of 2001 reveal that the diet of both hooded and harp seals are comprised of relatively few prey taxa. In both harp and hooded seal species, pelagic amphipods of the genus Parathemisto, the squid Gonatus fabricii, polar cod (Boreogadus saida) and capelin (Mallotus villosus) constituted 63%–99% of the observed diet
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biomass, irrespective of sampling period. Based on a simple 5 layer trophic pyramid (Heldal et al., 2003), the species determined by Haug et al. (2004) to dominate in the diets of Arctic seals (trophic level 5) are from trophic level 2 (amphipods), trophic level 3 (cephalopods, capelin) and trophic level 4 (polar cod). Differences in the relative dietary mix of these prey species and the clear importance of low trophic level prey in the diets of Arctic seals thus may explain why BCF values reported for Arctic seals are not substantially higher than their prey species. In comparison, BCFs for harbour porpoise from the Barents and Norwegian Seas are reported to be 165 ± 5 (Heldal et al., 2003) suggesting that harbour porpoises feed on a diet consisting of a larger proportion of higher trophic level species. Concerning the importance of diet selection processes, Haug et al. (2004) also report that the relative contribution of prey species to the diet varied both with seal species and sampling period/area, and there were large differences in dietary composition among individuals. In a related study, Christiansen et al. (2004) report that there are large differences among individual seals in their gastric properties (stomach temperature, acidity, pepsin concentration), properties related to the breakdown and assimilation of food, and hence may influence the transfer of radiocaesium from the digestive tract into the body. Differences were particularly pronounced in animals with body weights less than 100 kg which corresponds to the majority of individuals reported on in the present study. Their findings further indicate large differences in the feeding mode and diet composition of individuals: differences that would further be expected to influence biomagnification factors for radiocaesium in Arctic seals. Despite the complex array of sources of variation, and limited knowledge of the physiological and ecological processes controlling radiocaesium bioaccumulation, comparison of our more recent findings with earlier studies confirms that radiocaesium bioaccumulation factors in seals inhabiting different sub-regions of the European Arctic are generally similar. Furthermore, we suggest that the diets of Arctic seals, rich in species from lower trophic levels, lead to relatively low BCF values in these marine mammals. Clearly, to fully appreciate the importance of diet selection as a factor influencing biomagnification, diet composition and radiocaesium activity concentration must be examined simultaneously in a statistically relevant number of individuals. However, our findings would suggest that there is a strong effect of diet selection on radiocaesium bioaccumulation for seals and, to some degree, the levels found in NE Greenland seals reflect the levels found in prey items from their habitat areas, as confirmed in Haug et al. (2004) and Christiansen et al. (2004). Finally, the data provide further verification that the radiocaesium levels remain low throughout the European Arctic in accordance with expectations.
Acknowledgements This research was funded by Akvaplan-niva AS (Norway), the Institute of Marine Research (Norway) and the Radiation and Nuclear Safety Authority (Finland).
References Aarkrog, A. (1994). Radioactivity in polar regions – main sources. Journal of Environmental Radioactivity 25, 21–35.
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Aarkrog, A. (1997a). Doses to the Arctic Population. In: Materials of 3th International Conference on Environmental Radioactivity in the Arctic. Tromsø, pp. 113–115. Aarkrog, A. (1997b). AMAP Greenland 1994–1996. Environmental Project No. 356, pp. 211–239. Aarkrog, A., Dahlgaard, H., Nielsen, S.P. (2000). Environmental radioactive contamination in Greenland: A 35 years retrospect. The Science of the Total Environment 245, 233–248. AMAP (1998). Arctic Pollution Issues. AMAP Assessment Report. Arctic Monitoring and Assessment Programme (AMAP). Oslo, Norway, 859+xii pp. AMAP (2002). Persistent Organic Pollutants in the Arctic. AMAP Assessment 2002. Anderson, S.S., Livens, F.R., Singleton, D.L. (1990). Radionuclides in grey seals. Marine Pollution Bulletin 21, 343–345. Born, E.W., Dahlgaard, H., Riget, F., Dietz, R., Øien, N., Haug, T. (2002). Regional variation of caesium-137 in minke whales Balaenoptera acutorostrata from West Greenland, the Northeast Atlantic and the North Sea. Polar Biology 25, 907–913. Calmet, D., Woodhead, D., Andre, J.M. (1992). 210 Pb, 137 Cs, and 40 K in three species of porpoises caught on the eastern tropical Pacific Ocean. Journal of Environmental Radioactivity 15, 153–169. Carroll, J., Wolkers, H., Andersen, M., Rissanen, K. (2002). Bioaccumulation of radiocaesium in Arctic seals. Marine Pollution Bulletin 44, 1366–1371. Carroll, M.L., Carroll, J. (2003). The Arctic Seas. In: Black, K.D., Shimmield, G.B. (Eds.), Biogeochemistry of Marine Systems. Blackwell, Oxford, pp. 127–147. Christiansen, J.S., Gildberg, A., Nilssen, K.T., Lindblom, C., Haug, T. (2004). The gastric properties of free-ranging harp (Pagophilus groenlandicus (Erxleben, 1777)) and hooded (Cystophora cristata (Erxleben, 1777)) seals. ICES Journal of Marine Science 61, 287–292. Dahlgaard, H. (1995). On Tc-99, Cs-137 and Sr-90 in the Kara Sea. In: Strand, P., Cooke, A. (Eds.), Environmental Radioactivity in the Arctic. Norwegian Radiation Protection Authority, Østerås, pp. 91–95. Fisher, N.S., Fowler, S.W., Boisson, F., Carroll, J., Rissanen, K., Salbu, B., Sazykina, T.G., Sjoeblom, K.-L. (1999). Bioconcentration factors and sediment partition coefficients in Arctic seas subject to contamination from dumped nuclear wastes. Environmental Science and Technology 33, 1979–1982. Fisk, A.T., Hobson, K.A., Norstrom, R.J. (2001). Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwest polynya marine food web. Environmental Science and Technology 35, 732–738. Fowler, S.W. (1982). Biological transfer and transport processes. In: Kullenberg, G. (Ed.), Pollutant Transfer and Transport in the Sea, vol. II. CRC Press, Inc., Boca Raton, FL, pp. 1–65. Haug, T., Nilssen, K.T., Lindblom, L. (2004). Feeding habitats of harp and hooded seals in drift ice waters along the east coast of Greenland in summer and winter. Polar Research 23 (1), 35–42. Heldal, H.E., Føyn, L., Varskog, P. (2003). Bioaccumulation of 137 Cs in pelagic food webs in the Norwegian and Barents Seas. Journal of Environmental Radioactivity 65, 177–185. Kasamatsu, F., Ishikawa, Y. (1997). Natural variation of radionuclide 137 Cs concentrations in marine organisms with special reference to the effect of food habits and trophic level. Marine Ecology Progress Series 160, 109–120. Kershaw, P.J., Baxter, A. (1995). The transfer of reprocessing wastes from north-west Europe to the Arctic. Deep-Sea Research II 42, 1413–1448. Kershaw, P.J., Gurbutt, P., Woodhead, D., Leonard, K., Rees, J. (1997). Estimates of fluxes of 137 Cs in northern waters from recent measurements. The Science of the Total Environment 202, 211–223. Matishov, D.G., Matishov, G.G. (2004). Radioecology in Northern European Seas. Springer-Verlag, New York, 335 pp. Matishov, G.G., Matishov, D.G., Namjatov, A.E., Smith, J.N., Carroll, J., Dahle, S. (2002). Radioactivity near the sunken submarine ‘Kursk’ in the southern Barents Sea. Environmental Science and Technology 36 (9), 1919– 1922. Rissanen, K., Ikäheimonen, T.K., Matishov, D., Matishov, G.G. (1997). Radioactivity levels in fish, benthic fauna, seals and sea birds collected in the Northwest Arctic of Russia. Radioprotection – Colloques 32 (C2), 323–331. Rissanen, K., Pempkowiak, J., Ikäheimonen, T.K., Matishov, D.G., Matishov, G.G. (1999). 137 Cs, 239,240 Pu, 90 Sr and selected metal concentrations in organs of Greenland seal pups in the White Sea area. In: The 4th International Conference on Environmental Radioactivity in the Arctic. Edinburgh, Scotland, September 20–23. Rowan, D.J., Rasmussen, J.B. (1994). Bioaccumulation of radiocaesium by fish: The influence of physicochemical factors and trophic structure. Canadian Journal of Fisheries and Aquatic Sciences 51, 2388–2410.
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Strand, P., Balonov, M., Aarkrog, A., Bewers, M.J., Howard, B., Salo, A., Tsaturov, Y.S. (1997). Arctic Pollution Issues: Radioactive Contamination. Norwegian Radiation Protection Authority, Østerås. Watson, W.S., Sumner, D.J., Baker, J.R., Kennedy, S., Reid, R., Robinson, I. (1999). Radionuclides in seals and porpoises in the coastal waters around the UK. The Science of the Total Environment 234, 1–13. WWF (2004). A Biodiversity Assessment of the Barents Sea Ecoregion. WWF Arktisprogrammet, WWF-Norge og WWF-Russland. Available at http://www.wwf.no. Zhao, X., Wang, W.-X., Yu, K.N., Lam, P.K.S. (2001). Biomagnification of radiocesium in a marine piscivorous fish. Marine Ecology – Progress Series 222, 227–237.
Bioaccumulation of radiocaesium in Arctic seals from Northeast Greenland JoLynn Carrolla,* , Kristina Rissanenb , Tore Haugc a Akvaplan-niva, Polar Environmental Centre, Tromsø, Norway b URadiation and Nuclear Safety Authority, Helsinki, Finland c Institute of Marine Research, Tromsø, Norway
Abstract Seals are high trophic level feeders that bioaccumulate many contaminants to a greater degree than most lower trophic level organisms. Their trophic status in the marine food web and wide-spread distribution make seals useful sentinels of arctic environmental change. In 1999 and 2000 seals were captured from the northeast coast of Greenland (75– 80◦ N) in order to document the levels and bioaccumulation potential of radiocaesium in the high latitude seal species: harp, ringed, and hooded seals. The results are compared with previous studies in order to assess geographic differences in bioaccumulation for Arctic seals. Concentrations of 137 Cs were determined in muscle, liver and kidney samples from a total of 25 juvenile and 3 adult seals. The mean concentration in muscle and liver samples for all animals was 0.36 ± 0.14 Bq/kg f.w. and 0.26 ± 0.08 Bq/kg f.w. The results are consistent with previous studies indicating low levels of radiocaesium in Arctic seals in response to a long term trend of decreasing levels of 137 Cs in the Greenland Sea region. Comparing levels in muscle tissue among the different seal species, the 137 Cs activity concentration of harp (0.36 ± 0.14 Bq/kg f.w.) and hooded seals (0.37 ± 0.14 Bq/kg f.w.) are similar within uncertainty limits while average concentrations in ringed seals are slightly lower (0.2 Bq/kg f.w.). Bioconcentration factors (BCFs) for the seals (30–110) correspond well with the variety of prey consumed by seals in this region indicating that diet selection is a dominant factor controlling bioaccumulation of radiocaesium in these Arctic seals. Keywords: Bioaccumulation, Radiocaesium, Seals, Greenland
1. Introduction Seals are among the most quantitatively important mammals in the upper part of the marine food chain, along with whales, walrus and polar bear (WWF, 2004). Due to the importance of seals in subsistence diets of Arctic indigenous peoples, they are a major focus of several on-going monitoring and protection efforts (AMAP, 2002). The results of this investigation provide critical information on concentrations of the radionuclide 137 Cs (radiocaesium) which is among the more pervasive elements found in the Arctic. * Corresponding author. Address: Akvaplan-niva AS, Polar Environmental Centre, Tromsø, phone: (+47) 7775 0314 +; fax: (+47) 7775 0301 +; e-mail: [email protected]
RADIOACTIVITY IN THE ENVIRONMENT VOLUME 8 ISSN 1569-4860/DOI 10.1016/S1569-4860(05)08018-6
© 2006 Elsevier Ltd. All rights reserved.
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The main sources of radiocaesium to the Arctic are discharges from Europe’s nuclear reprocessing facilities. It is estimated that these facilities have contributed 10–15 PBq to the Arctic Ocean as compared to global fallout and Chernobyl which have contributed 4.1 PBq and 1–5 PBq, respectively (Aarkrog, 1994; Strand et al., 1997). Discharges from Sellefield (UK) and La Hague (France), the two largest reprocessing facilities, enter the Irish Sea and English Channel, respectively. After mixing with Chernobyl-laden water from the Baltic Sea in the North Sea, the plume of radiocaesium is transferred further northward by the Norwegian Coastal Current. Once in the Norwegian Sea, the caesium-laden current bifurcates with one branch leading into the Barents Sea (Barents Sea Overflow Current) and the other branch (West Spitzbergen Current) traversing around the west coast of Svalbard (Kershaw and Baxter, 1995; Kershaw et al., 1997; Heldal et al., 2003) (Fig. 1). Part of the northward flowing West Spitzbergen Current detaches and is re-circulated within the Greenland Sea. The transport time for radiocaesium from the North Sea into the Greenland Sea has been estimated to be on the order of 5 years (Dahlgaard, 1995). This caesium enriched water further mixes with lower concentration Arctic Ocean water entering the North Atlantic via the Fram Strait. A number of regional sources of radionuclides exist in the adjacent Norwegian, Barents, and Kara Seas. These secondary sources of radioactive contamination to northern European waters include fluvial inputs from nuclear facilities on the Ob and Yenisey Rivers, point source inputs from radioactive waste dump sites and nuclear test sites on the Russian coastline. Included as well are the nuclear operations related to the military-industrial complex in the Kola Peninsula. Several nuclear accidents have occurred in the region (AMAP, 1998; Matishov et al., 2002) and on-going activities in the region have been identified as possibili-
Fig. 1. Generalized pathway of radiocaesium transport from Sellefield (UK) and La Hague (France) into the Arctic Ocean. In Greenland waters, radiocaesium from Sellefield is returning from the Arctic Ocean. Seal bioconcentration factors (BCF) among different sub-regions of the European Arctic are also shown.
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ties of accidents in the future (Strand et al., 1997). Of greatest concern are the Kola nuclear power plant reactors, nuclear submarines or icebreakers, waste disposal, nuclear weapons or military activities in Murmansk and Archangelsk regions, Novaya Zemlya installations, and military-industrial sites located within catchment areas of the rivers Ob and Yenisey. Levels of radioceasium around northeast Greenland began declining in the mid-1970s in response to a decline in discharges from Sellefield four years earlier (Matishov and Matishov, 2004). During the early to mid-1970s surface seawater concentrations in the Greenland Sea above 65◦ N were on the order of 9 Bq/m3 . In the early to mid-1990s, concentrations had decreased to approximately 7 Bq/m3 (Aarkrog et al., 2000). Among the wide variety of radionuclides present in the Arctic environment, radiocaesium is the only radionuclide that has been shown to biomagnify through marine food webs (Calmet et al., 1992; Kasamatsu and Ishikawa, 1997; Watson et al., 1999; Heldal et al., 2003; Zhao et al., 2001). And it has been hypothesized that features unique to Arctic ecosystems lead to increased vulnerability for organisms from contaminant releases (Fisher et al., 1999; Carroll and Carroll, 2003). These features include: the seasonal and spatial focus of primary productivity, strong benthic-pelagic coupling, a prevalence of large mammals as apex predators, and relatively large amplitude fluctuations in the lipid cycle of some species. Few studies have been conducted on Arctic marine mammals and in particular for seals (Aarkrog et al., 2000; Rissanen et al., 1997; Carroll et al., 2002). Better knowledge is needed of the bioaccumulation potential of apex predators for a variety of species, habitats, and environmental conditions. The present study provides an opportunity to examine the levels and bioaccumulation potential for radiocaesium in harp, ringed, and hooded seals from NE Greenland. The data are used in conjunction with previous work to compare differences among Arctic seal populations from several locations. This knowledge will lead to more effective use of seals and other marine mammals as indicators of environmental change in Arctic marine monitoring programmes.
2. Methods 2.1. Field sampling A research vessel was used to search for harp, hooded, and bearded seals along the drift ice edge areas of the east coast of Greenland in Fall 1999 and Summer 2000 (Table 1). Animals were weighed to the nearest 1/2 kg and sex and sexual maturity (juveniles and adults) were determined. Sub-samples of seal muscle, liver, and kidney were removed and frozen at −20◦ C until analyses were performed. Ages of seals were estimated by counting of growth layers on teeth extracted from individuals as described in Haug et al. (2004). Samples were analyzed at the Radiation and Nuclear Safety Authority in Finland. Muscle, liver and kidney samples from individual seals were cleaned, cut into small pieces, dried at 105◦ C and homogenized. Each sample was placed in a Marinelli beaker or in 100 or 35 ml plastic jars. Samples were counted on a high-purity, low background, gamma spectrometer for time periods ranging from 900–6800 minutes. The spectrometer was calibrated using matrixmatched standards in a similar geometry.
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Table 1 Radiocaesium concentrations (Bq/kg f.w.) in seal muscle and liver tissue. Ringed, hooded, and harp seals were captured in October 1999 from Northeast Greenland Species
Weight (kg)
Age (yrs)
Sex
Muscle (Bq/kg f.w.)
Liver (Bq/kg f.w.)
Ringed Ringed Ringed Harp Harp Harp Harp Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded Hooded
21 58 47 62 58 54 32 36 43 205 36 39 43 56 35 45 32 27 38 41 34 66
<1 10 >20 1 2 1 <1 <1 <1 10 <1 <1 <1 <1 <1 <1 <1 <1 <1 <1 <1 1
M M M M M M M F F M M M M M M F F M M M F M
<0.2 0.2 ± 0.05 <0.2 0.39 ± 0.04 0.29 ± 0.06 0.30 ± 0.06 0.44 ± 0.05 0.25 ± 0.05 0.36 ± 0.09 0.44 ± 0.08 0.26 ± 0.07 0.45 ± 0.07 0.32 ± 0.05 0.72 ± 0.13 0.18 ± 0.04 <0.4 <0.2 <0.5 <0.3 0.37 ± 0.05 0.24 ± 0.04 0.40 ± 0.07
0.18 ± 0.03 0.32 ± 0.07 – 0.21 ± 0.05 <0.30 <0.13 0.36 ± 0.05 <0.17 0.32 ± 0.07 0.20 ± 0.04 0.16 ± 0.03 0.36 ± 0.06 0.24 ± 0.05 – <0.10 <0.20 – – – 0.20 ± 0.04 <0.24 –
Mean ± stdev Ringed
0.20 n=3
Mean ± stdev
0.36 ± 0.07
Harp Mean ± stdev
n=4 0.37 ± 0.15
Hooded
n = 15
Mean ± stdev All
0.36 ± 0.13 n = 22
0.25 ± 0.07 n=2
0.25 ± 0.08 n = 10 0.26 ± 0.08 n = 16
3. Results 3.1. Radiocaesium levels Samples of muscle, liver, and kidney taken from seals collected in 1999 and 2000 were analyzed as described in the previous section and are summarized in Table 1 and Table 2 respectively. The 137 Cs activity concentration of seal muscle for all animals (1999 and 2000 combined) was relatively low (mean = 0.37 ± 0.14 Bq/kg f.w.; n = 22). 137 Cs concentrations in liver were slightly lower than in muscle (mean = 0.26 ± 0.08 Bq/kg f.w.; n = 14).
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Table 2 Radiocaesium concentrations (Bq/kg f.w.) in muscle, liver and kidney tissue from hooded seals collected from Northeast Greenland in July 2000 Species
Weight (kg)
Age (yrs)
Sex
Muscle (Bq/kg f.w.)
Liver (Bq/kg f.w.)
Kidney (Bq/kg f.w.)
Hooded Hooded Hooded Hooded Hooded Hooded
75 81 70 88 90 139
2 2 4 5 8 16
M M M F F M
0.44 ± 0.05 0.22 ± 0.04 0.23 ± 0.04 0.60 ± 0.06 0.34 ± 0.05 0.59 ± 0.06
0.34 ± 0.04 <0.1 <0.1 0.34 ± 0.05 0.17 ± 0.03 0.26 ± 0.04
0.20 ± 0.04 0.11 ± 0.04 0.16 ± 0.04 0.23 ± 0.04 0.35 ± 0.06 0.23 ± 0.04
0.40 ± 0.17
0.28 ± 0.08
0.35 ± 0.06
Mean ± stdev
Kidney samples were taken only during the 2000 expedition, and contained 137 Cs in concentrations similar to liver (mean = 0.21 ± 0.08 Bq/kg f.w.; n = 6). Comparing levels in muscle tissue among the different seal species, the 137 Cs activity concentration of harp and hooded seals are similar within uncertainty limits while ringed seals contain significantly lower radiocaesium concentrations despite similarities in animal sizes among the three species examined (Table 1). However there were no corresponding differences in 137 Cs activity concentration in liver samples among the three species examined during the investigation. 3.2. Radiocaesium bioconcentration factors Bioconcentration factors (BCFs) normalize radiocaesium tissue levels for spatial and temporal differences in environmental concentrations. The bioconcentration factor (BCF) is defined as BCF = CORG (Bq/kg fresh weight)/CSW (Bq/kg), CORG = concentration in the organism, CSW = concentration in seawater. The BCFs for NE Greenland seals were calculated taking the radiocaesium concentration measurements in individual muscle tissue samples and dividing these by a seawater concentration of 6.6 Bq/m3 . The resulting range of BCF values is from 30–110 (Table 3). This seawater concentration was estimated by extrapolating the long-term linear trend of decreasing seawater concentrations as measured in the waters surrounding NE Greenland and described by Aarkrog et al. (2000). Aarkrog et al. (2000) report that the mean seawater concentration during 1990–1997 in NE Greenland between 70–65◦ N, 75–70◦ N and 80–75◦ N were 7.1 ± 2.2, 7.1 ± 1.8 and 7.1 ± 1.3, respectively. There is little change to our determined BCF values as a result of the extrapolated decrease in seawater concentrations from the early to late 1990s. Certainly these minor differences do not alter the overall conclusions of this investigation.
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Table 3 Bioconcentration factors (BCFs) in muscle tissue of marine mammals collected from different regions of the Northern European seas Location
Marine mammal
Time period
BCF value
Source
NE Greenland NE Svalbard White Sea/Kola Peninsula Greenland Barents/Norwegian Seas Svalbard Barents Sea
Seals Seals Seals Marine mammals Harbour porpoise Minke whales Minke whales
1999–2000 2000 1994–1995 1990–1997 1998–2000 1998 1998
30–110 34–130 60 ± 20 114 165 ± 5 70–150∗ 130–285∗
Present study Carroll et al., 2002 Rissanen et al., 1997 Aarkrog et al., 2000 Heldal et al., 2003 Born et al., 2002 Born et al., 2002
∗ Calculation made assuming a seawater concentration range of 2.0–4.4 Bq/kg for 137 Cs (Heldal et al., 2003).
4. Discussion 4.1. Radiocaesium levels in seals Seals living at the ice edge in the Greenland Sea are continuously exposed to radiocaesium. Conditions of chronic low level radioactive contamination, such as are present in the Greenland Sea today, lead to food chain transfer as the dominant pathway of exposure for marine organisms (Fowler, 1982; Rowan and Rasmussen, 1994; Zhao et al., 2001). Approximately 70% of the body burden of radiocaesium accumulates in muscle tissue with the additional 30% taken up by other parts of the organism (Anderson et al., 1990). Studies of dissected seal pups from Northwest Russia indicate that radiocaesium concentrations are highest in soft tissues (e.g. parathyroid gland, pancreas, cartilaginous tissues, ovaries) and lowest in bones and fat (Rissanen et al., 1999). Since radiocaesium levels in the seas surrounding the Arctic Ocean are currently very low, seals from NE Greenland would be expected to contain correspondingly low concentrations in their tissues and organs. Concentrations are highest in NE Greenland as compared to other sections of Greenland. This is a consequence of the influence of the recirculation currents originating from the West Spitzbergen Current which contain relatively high concentrations of radiocaesium derived mainly from the European reprocessing facilities (Aarkrog et al., 2000). The overall low mean radiocaesium concentration of 0.37 ± 0.14 Bq/kg in seal muscle, confirms the expectation that regional sources in addition to the main sources (reprocessing facilities, Chernobyl, global fallout) have thus far not had a significant impact on the marine ecosystem. Radiocaesium levels have not changed since 1990–1994 (0.40 ± 0.12 Bq/kg) and are in accordance with the long-term trend of slowly diminishing radiocaesium concentrations in seawater since 1970 (Aarkrog et al., 2000; Aarkrog, 1997a, 1997b). Concentrations in NE Greenland seals are slightly higher as compared to concentrations in seal pups taken from NE Svalbard during the same year (Spring 1999). In NE Svalbard the mean concentration for all animals was 0.23 ± 0.04 Bq/kg f.w. (n = 11) (Carroll et al., 2002). These differences mirror the higher radiocaesium concentrations detected in seawater from NE Greenland (∼6.6 Bq/m3 ) as compared to NE Svalbard (2.0–4.7 Bq/m3 ) and are
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a consequence of the greater influence of Europe’s nuclear reprocessing facilities on the waters surrounding Greenland as compared to Svalbard. 4.2. Radiocaesium bioconcentration in seals The bioaccumulation of radiocaesium in seals represents the outcome of many factors involving a combination of physiological factors, such as absorption efficiency, and ecological factors including diet selection, feeding rates, and prey availability. Migration patterns will also determine the amount of radiocaesium accumulated from food and subsequently retained in the body due to variations in seawater concentrations along the main transport pathway to the Arctic from the main source areas (Fig. 1). Comparing different regions of the Arctic, seals have the lowest BCF values, followed by porpoises, while whales generally have the highest BCF values (Table 3). The BCFs reported for seals from NE Greenland and NE Svalbard further agree well with the value reported previously by Aarkrog et al. (2000) for marine mammals from all of Greenland’s coastal waters (BCF = 114) indicating that these various data sets provide a consistent picture of radiocaesium biouptake in Arctic seals. Among the wide variety of radionuclides present in the Arctic environment, radiocaesium can biomagnify through marine food chains (Anderson et al., 1990; Kasamatsu and Ishikawa, 1997; Fisk et al., 2001; Zhao et al., 2001). Biomagnification of radiocaesium implies that the trophic status of primary prey items is an important factor affecting the radiocaesium activity concentration of seals. As a result, a clear effect of diet selection on radiocaesium bioaccumulation would be expected. BCFs reported for prey items from the Barents and Norwegian Seas (Heldal et al., 2003) and in the waters surrounding Greenland (Aarkrog et al., 2000) for omnivorous fish, benthic organisms, and carnivorous fish are within an approximate range of 10–100. Thus the relatively low BCF values obtained for seals from the European Arctic indicate only a slight enhancement of radiocaesium in relation to prey species (Table 3). Given that life-times of seals (∼30 years) are significantly longer than for prey species (∼5–15 years) we would expect that over time, seals would bioaccumulate increasingly high levels of radiocaesium resulting in correspondingly higher BCF values. While this is apparently not the case for Arctic seals, studies of other marine mammals report a clear increase in bioaccumulation relative to potential lower trophic level prey items, for example, Harbour porpoises (BCF = 165 ± 5) and Minke whales (BCF = 130–285) from the Barents Sea (Table 3). Yet these findings are in contrast to those of Aarkrog et al. (2000) who report no significant differences in radiocaesium contamination between whales and seals taken from Greenland waters. The resulting low BCF values for seals from NE Greenland may be related to the relatively young age of seals in the present study in combination with diet selection factors. The BCF value would be expected to be relatively low if the diet selection of seals consists of organisms relatively low on the trophic pyramid. Analyses of stomach and intestinal contents from hooded and harp seals captured in the pack ice belt of the Greenland Sea in summer (July–August) of 2000 and winter (February–March) of 2001 reveal that the diet of both hooded and harp seals are comprised of relatively few prey taxa. In both harp and hooded seal species, pelagic amphipods of the genus Parathemisto, the squid Gonatus fabricii, polar cod (Boreogadus saida) and capelin (Mallotus villosus) constituted 63%–99% of the observed diet
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biomass, irrespective of sampling period. Based on a simple 5 layer trophic pyramid (Heldal et al., 2003), the species determined by Haug et al. (2004) to dominate in the diets of Arctic seals (trophic level 5) are from trophic level 2 (amphipods), trophic level 3 (cephalopods, capelin) and trophic level 4 (polar cod). Differences in the relative dietary mix of these prey species and the clear importance of low trophic level prey in the diets of Arctic seals thus may explain why BCF values reported for Arctic seals are not substantially higher than their prey species. In comparison, BCFs for harbour porpoise from the Barents and Norwegian Seas are reported to be 165 ± 5 (Heldal et al., 2003) suggesting that harbour porpoises feed on a diet consisting of a larger proportion of higher trophic level species. Concerning the importance of diet selection processes, Haug et al. (2004) also report that the relative contribution of prey species to the diet varied both with seal species and sampling period/area, and there were large differences in dietary composition among individuals. In a related study, Christiansen et al. (2004) report that there are large differences among individual seals in their gastric properties (stomach temperature, acidity, pepsin concentration), properties related to the breakdown and assimilation of food, and hence may influence the transfer of radiocaesium from the digestive tract into the body. Differences were particularly pronounced in animals with body weights less than 100 kg which corresponds to the majority of individuals reported on in the present study. Their findings further indicate large differences in the feeding mode and diet composition of individuals: differences that would further be expected to influence biomagnification factors for radiocaesium in Arctic seals. Despite the complex array of sources of variation, and limited knowledge of the physiological and ecological processes controlling radiocaesium bioaccumulation, comparison of our more recent findings with earlier studies confirms that radiocaesium bioaccumulation factors in seals inhabiting different sub-regions of the European Arctic are generally similar. Furthermore, we suggest that the diets of Arctic seals, rich in species from lower trophic levels, lead to relatively low BCF values in these marine mammals. Clearly, to fully appreciate the importance of diet selection as a factor influencing biomagnification, diet composition and radiocaesium activity concentration must be examined simultaneously in a statistically relevant number of individuals. However, our findings would suggest that there is a strong effect of diet selection on radiocaesium bioaccumulation for seals and, to some degree, the levels found in NE Greenland seals reflect the levels found in prey items from their habitat areas, as confirmed in Haug et al. (2004) and Christiansen et al. (2004). Finally, the data provide further verification that the radiocaesium levels remain low throughout the European Arctic in accordance with expectations.
Acknowledgements This research was funded by Akvaplan-niva AS (Norway), the Institute of Marine Research (Norway) and the Radiation and Nuclear Safety Authority (Finland).
References Aarkrog, A. (1994). Radioactivity in polar regions – main sources. Journal of Environmental Radioactivity 25, 21–35.
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Aarkrog, A. (1997a). Doses to the Arctic Population. In: Materials of 3th International Conference on Environmental Radioactivity in the Arctic. Tromsø, pp. 113–115. Aarkrog, A. (1997b). AMAP Greenland 1994–1996. Environmental Project No. 356, pp. 211–239. Aarkrog, A., Dahlgaard, H., Nielsen, S.P. (2000). Environmental radioactive contamination in Greenland: A 35 years retrospect. The Science of the Total Environment 245, 233–248. AMAP (1998). Arctic Pollution Issues. AMAP Assessment Report. Arctic Monitoring and Assessment Programme (AMAP). Oslo, Norway, 859+xii pp. AMAP (2002). Persistent Organic Pollutants in the Arctic. AMAP Assessment 2002. Anderson, S.S., Livens, F.R., Singleton, D.L. (1990). Radionuclides in grey seals. Marine Pollution Bulletin 21, 343–345. Born, E.W., Dahlgaard, H., Riget, F., Dietz, R., Øien, N., Haug, T. (2002). Regional variation of caesium-137 in minke whales Balaenoptera acutorostrata from West Greenland, the Northeast Atlantic and the North Sea. Polar Biology 25, 907–913. Calmet, D., Woodhead, D., Andre, J.M. (1992). 210 Pb, 137 Cs, and 40 K in three species of porpoises caught on the eastern tropical Pacific Ocean. Journal of Environmental Radioactivity 15, 153–169. Carroll, J., Wolkers, H., Andersen, M., Rissanen, K. (2002). Bioaccumulation of radiocaesium in Arctic seals. Marine Pollution Bulletin 44, 1366–1371. Carroll, M.L., Carroll, J. (2003). The Arctic Seas. In: Black, K.D., Shimmield, G.B. (Eds.), Biogeochemistry of Marine Systems. Blackwell, Oxford, pp. 127–147. Christiansen, J.S., Gildberg, A., Nilssen, K.T., Lindblom, C., Haug, T. (2004). The gastric properties of free-ranging harp (Pagophilus groenlandicus (Erxleben, 1777)) and hooded (Cystophora cristata (Erxleben, 1777)) seals. ICES Journal of Marine Science 61, 287–292. Dahlgaard, H. (1995). On Tc-99, Cs-137 and Sr-90 in the Kara Sea. In: Strand, P., Cooke, A. (Eds.), Environmental Radioactivity in the Arctic. Norwegian Radiation Protection Authority, Østerås, pp. 91–95. Fisher, N.S., Fowler, S.W., Boisson, F., Carroll, J., Rissanen, K., Salbu, B., Sazykina, T.G., Sjoeblom, K.-L. (1999). Bioconcentration factors and sediment partition coefficients in Arctic seas subject to contamination from dumped nuclear wastes. Environmental Science and Technology 33, 1979–1982. Fisk, A.T., Hobson, K.A., Norstrom, R.J. (2001). Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwest polynya marine food web. Environmental Science and Technology 35, 732–738. Fowler, S.W. (1982). Biological transfer and transport processes. In: Kullenberg, G. (Ed.), Pollutant Transfer and Transport in the Sea, vol. II. CRC Press, Inc., Boca Raton, FL, pp. 1–65. Haug, T., Nilssen, K.T., Lindblom, L. (2004). Feeding habitats of harp and hooded seals in drift ice waters along the east coast of Greenland in summer and winter. Polar Research 23 (1), 35–42. Heldal, H.E., Føyn, L., Varskog, P. (2003). Bioaccumulation of 137 Cs in pelagic food webs in the Norwegian and Barents Seas. Journal of Environmental Radioactivity 65, 177–185. Kasamatsu, F., Ishikawa, Y. (1997). Natural variation of radionuclide 137 Cs concentrations in marine organisms with special reference to the effect of food habits and trophic level. Marine Ecology Progress Series 160, 109–120. Kershaw, P.J., Baxter, A. (1995). The transfer of reprocessing wastes from north-west Europe to the Arctic. Deep-Sea Research II 42, 1413–1448. Kershaw, P.J., Gurbutt, P., Woodhead, D., Leonard, K., Rees, J. (1997). Estimates of fluxes of 137 Cs in northern waters from recent measurements. The Science of the Total Environment 202, 211–223. Matishov, D.G., Matishov, G.G. (2004). Radioecology in Northern European Seas. Springer-Verlag, New York, 335 pp. Matishov, G.G., Matishov, D.G., Namjatov, A.E., Smith, J.N., Carroll, J., Dahle, S. (2002). Radioactivity near the sunken submarine ‘Kursk’ in the southern Barents Sea. Environmental Science and Technology 36 (9), 1919– 1922. Rissanen, K., Ikäheimonen, T.K., Matishov, D., Matishov, G.G. (1997). Radioactivity levels in fish, benthic fauna, seals and sea birds collected in the Northwest Arctic of Russia. Radioprotection – Colloques 32 (C2), 323–331. Rissanen, K., Pempkowiak, J., Ikäheimonen, T.K., Matishov, D.G., Matishov, G.G. (1999). 137 Cs, 239,240 Pu, 90 Sr and selected metal concentrations in organs of Greenland seal pups in the White Sea area. In: The 4th International Conference on Environmental Radioactivity in the Arctic. Edinburgh, Scotland, September 20–23. Rowan, D.J., Rasmussen, J.B. (1994). Bioaccumulation of radiocaesium by fish: The influence of physicochemical factors and trophic structure. Canadian Journal of Fisheries and Aquatic Sciences 51, 2388–2410.
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Strand, P., Balonov, M., Aarkrog, A., Bewers, M.J., Howard, B., Salo, A., Tsaturov, Y.S. (1997). Arctic Pollution Issues: Radioactive Contamination. Norwegian Radiation Protection Authority, Østerås. Watson, W.S., Sumner, D.J., Baker, J.R., Kennedy, S., Reid, R., Robinson, I. (1999). Radionuclides in seals and porpoises in the coastal waters around the UK. The Science of the Total Environment 234, 1–13. WWF (2004). A Biodiversity Assessment of the Barents Sea Ecoregion. WWF Arktisprogrammet, WWF-Norge og WWF-Russland. Available at http://www.wwf.no. Zhao, X., Wang, W.-X., Yu, K.N., Lam, P.K.S. (2001). Biomagnification of radiocesium in a marine piscivorous fish. Marine Ecology – Progress Series 222, 227–237.