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Environ Monit Assess (2007) 128:329-341 DO1 10.1007/~10661-006-93I64 ORIGINAL ARTICLE -

Radionuclide Concentrations in Benthic Invertebrates from Amchitka and Kiska Islands in the Aleutian Chain, Alaska

Joanna Burger Michael Gochfeld Stephen C. Jewett

Received: 8 March 2006 /Accepted: 8 May 2006 1 Published online: 21 October 2006 0 Springer Science + Business Media B.V. 2006

Abstract Concentrations of 13 radionuclides and there were no differences among species. The 1291, 60co, 152~~,90sr, 99~~,241~~, 238pu, 239249pu, only radionuclides where composite samples were 234~,235~, 236U, 238~were examined in seven above the Minimum Detectable Activity (MDA) were species of invertebrates from Amchitka and Kiska 137Cs, 241Am, 239.249~~, 234~, 235~, 236U, and 238U. Islands, in the Aleutian Chain of Alaska, using Green sea urchin (Strongylocentrotus polyacanthus), gamma spectroscopy, inductively coupled plasma giant (Cyptochiton stefferi), plate mass spectroscopy, and alpha spectroscopy. Amchitka (Tectura scum) and giant Pacific (Enter- Island was the site of three underground nuclear test octopus dojleini) were only tested for 13'cs; octopus (1965-1971), and we tested the null hypotheses that was the only species with detectable levels of '37~s there were no differences in radionuclide concentra- (0.262 i 0.029 Bqkg, wet weight). Only rock jingle tions between Amchitka and the reference site (Kiska) (Pododesmus macroschisma), blue ( trossufus) and horse mussel (Modiofus modiofus) were analyzed for the actinides. There were no J. Burger (lXI) interspecific differences in 241~mand 239U9~,and Division of Life Sciences, Rutgers University, almost no samples above the MDA for 238~~and 604 Allison Road, 236~.Horse had significantly higher concen- Piscataway, NJ 08854-8082, USA e-mail: [email protected] trations of 234~(0.844 f 0.804 Bqlkg) and 238~ (0.730 h 0.646) than the other species (both isotopes J. Burger. M. Gochfeld S. C. Jewett are naturally occurring). There were no differences in Cobsortium for Risk Evaluation with Stakeholder actinide concentrations between Amchitka and Kiska. Participation (CRESP), and Environmental and Occupational Health Sciences Institute (FiOHSI), In general, radionuclides in invertebrates from Piscataway, NJ, USA Amchitka were similar to those from uncontaminated sites in the Northern Hemisphere, and below those M. Gochfeld from the contaminated Irish Sea. There is a clear Environmental and Occupational Medicine, UMDNJ-Robert Wood Johnson Medical School, research need for authors to report the concentrations Piscataway, NJ, USA of radionuclides by species, rather than simply as '', for comparative purposes in determining S. C. Jewett geographical patterns, understanding possible effects, School of Fisheries and Sciences, University of Alaska, Fairbanks, and for estimating risk to humans from consuming AK 99775-7220, USA different biota.

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Environ Monit Assess (2007) 128:329-341

Keywords Radionuclides Radiocesium. Actinides. well as exposure due to dumping by the Former Invertebrates .Octopus . Mussels Rock jingles - Soviet Union (Togawa et al., 1999; Yamada, Aono, & Aleutians Arnchitka Kiska Hirano, 1999; Lystsov, Murzin, & Nezhdanov, 1999; Matishov, Matishov, Anisimova, Dzhenyuk, & Zuev, 2001). Some of this biomonitorbg is ongoing near 1 Introduction decommissioned nuclear power plants and reprocess- ing plants (e.g., Sellafield in the United Kingdom, Radionuclides enter the environment from natural Sanchez-Cabeza & Molero, 2000; in Taiwan, Hung, geologic sources and from fallout from historic nucle- Huang, & Shao, 1998). There is also interest in ar weapons testing (Aarkrog, 2003; Duran, Povinec, assessing radionuclide concentrations in organisms Fowler, Airey, & Hong, 2004), from nuclear facility near nuclear waste facilities, including nuclear testing and submarine accidents (Baeza et al., 1994; Cooper et sites. al., 1998; Livingston & Povinec, 2000; UNSCEAR, In this paper we examine the concentrations of a 2000; Sanchez-Cabeza & Molero, 2000; Amundsen et suite of radionuclides in several invertebrates in the al., 2002; Aumento, Donne & Eroe, 2005), and &om marine environment around Amchitka Island in the discarded nuclear wastes (Fisher et al., 1999; IAEA, Aleutian chain of Alaska. This paper reports on part of 1999). Over 500 atmospheric nuclear weapons tests the biologic study carried out by the Consortium for were conducted from 1945-1980, primarily in the Risk Evaluation with Stakeholder Participation Northern Hemisphere (UNSCEAR, 2000). The dis- (CRESP). CRESP is a multi-university, multi-disci- posal of large quantities of radioactive wastes in the plinary organization, assisting the U.S. Department of Arctic Seas by the former Soviet Union has prompted Energy (DOE) in pursuing remediation of nuclear interest in radionuclides in the Bering Sea ecosystem wastes generated during the Cold War manufacture and (Fisher et al., 1999). Some radionuclide concentra- testing of nuclear weapons. Even though the inverte- tions, such as the plutonium found in mussels in some brate community in the Aleutians is mostly inconspic- regions, however, are due mainly to upwelling of uous, compared to other regiona(O'Clair, 1977), some mid-depth waters from the Pacific Ocean, not to invertebrates could prove valuable as indicators of radioactive dumping in the region local (Farrington, radionuclide exposure because they are relatively Davis, Tripps, Phelphs, & Galloway, 1987). The sedentary, and occupy different trophic groups. More- potential for human health and environmental effects over some are consumed as part of regional subsis- fiom consumption of radionuclides in marine organ- tence diets (APIA, 2002; Patrick, 2002; Hamrick & isms is clear, particularly for I3'cs and 239~~(Moscati Smith, 2003). & Erdrnann, 1974; Shenber, Elshamis, Elkikli, & We test the null hypotheses that 1) there were no Elayan, 1999). interspecific differences in radionuclide concentrations, Increasingly, the public, regulators, managers and and 2) there were no differences in radionuclide policy makers are interested in assessing the health of concentrations between Amchitka and a reference site ecosystems, the food chain, and human foods. Because (Kiska Island). Amchitka was the site of three under- of the importance of fish and shellfish consumption ground nuclear tests from 1965 to 1971. Although throughout the world, and the occurrence of atrno- radionuclide concentrations were assessed in marine spheric deposition of radionuclides into marine envi- biota in the early 1970s (Memtt & Fuller, 1977), little ronments, a number of monitoring programs for testing has occurred since then, although Dasher et al. radionuclides have been established in Asia (Duran et (2002) assessed radionuclide concentrations in terres- al., 2004), in the Sea of Japan (Togawa, Povinec, & trial biota. Pettersson, 1999; JCAC, 2003, 2004), in the Irish Sea These data can be used to assess whether the (RPII, 2003, 2004), in the French Mediterranean subsistence foods and commercial fish are safe for (Charmasson, Barker, Calmet, Pruchon, & Thebault, consumption, to establish a baseline for future com- 1999), and in the Black Sea (Bologa, 2000). Other parison, and to determine whether the concentrations biomonitoring programs have been established to found in fish and birds at Amchitka are similar to those evaluate possible exposure from nuclear facility found in other regions of the Northern Hemisphere. operations (Poon & Au, 2002; Shinohara, 2004), as This work is part of a larger multi-disciplinary project by CRESP to provide the infbmation to assure the Page, Biswas, Lahr, & Pulpan, 1991; Eichelberger, protection of human health and the environment, Freymuella, Hill & Patrick, 2002; Jew* 2002; and to provide a baseline for monitoring in the context Patrick, 2002). of a long-term stewardship plan for Arnchitka Arnchitka Island was a military base oppming the (Fowas, Burger, Kosson, Gwhfeld, & Barnes, Japanese occupation of Kiska Island in Wdd War II. 2005, Powers, Burger, Usson, & Godrfeld, 2006; In the 1960s Amchitka was chosen for underground Burger, Gochfeld, Kosson, & Powers, 2006). Further, nuclear tests over the objdons of local people and radionuclide concentrations in benthic organisms fdgngovernments (O'Nei11,1994, Kohlhoff, 2002). living at high latitudes have been poorly investigated The remoteness of Amhitka, the tectonic activity (Matishov & Mtishov, 2004), and the pentstudy (which might 'hide' a nuclar test signahrre in seismic coniriiutes to the overall knowledge of radionuclides noise), and its proximity to the Soviet Union were in invertebrates from this region. hrsin its selection (?bhlhoff, 2002). There were three nuclear htsin 1965, 1969, and 197 1. Carmikin (abut 5 Mt in 1971) was the last and largest U. S. 2 Study W~Band Methods underground test. The three Amchitka test shots accounted for about 16% of the total energy released 2.1 Smdy sites hnthe U.S. underground testing program (Robbins, Makhijani, & Yih, 1991; Norris & Arkin, 1998; DOE, Arnchitka Island (5 1.5O N lat; 179' E long) and Kiska 2000). The relevant source tern information is Island (about 120 km to the west, I 77S0 E Long) in classified and unavailable to the public and the the western Aleutian Chain of Alaska, are psrt of the authors. The releases of radiation to the surface were Alaska Maritime National Wildlife Refuge. The not considered to pose serious health or ecological islands are bordered on the south by the North Pacific risks at the time (Seymour & Nelson, 1977; Faller & and on the north by the Bering Sea (Tipre 1). The Farmer, 1998), and recent studies by Dasher et al. marine biological resow in the regi0n.m of high (2002) did not indicate any current surface contami- value in cultural (including subsistence), commercial, nation. The infrastructure on the island (buildings, and ecological terms (NRC, 1996; Jewett, 2002). It is ds,wells) was removed by the Depment of dso one of the most seismically, tectonically and Energy (DOE) during remediation of s&e contam- volcanically active regions of the world (Jacob, 1984; ination in 2001. There is no current technology for

Figure 1 Map of Alaska showing low~tions of Aleut villages that took part in the mhpmcess, as weH as Arnchitka and Kiska Islands.

Unalaska -/' \\- Mlkolskl Kiska Mak I Amchitka I Environ Monit Assess (2007) 1283329-341 remediating the test cavities, to inactivate or entrap ent marine zones, fkom intertidal (blue mussels, the radiation, or over the long term, to interdict its limpets), to benthic (giant chiton, rock jingles, horse transport by ground water through fissures and porous mussels, , sea urchins). rock to the sea. Sea urchins, plate limpets (called Chinese Hats by The intense heat of the detonations at Amchitka Aleut subsistence hunters), and blue mussels were presumably melted the rock, and trapped much of the collected by both the Aleut and scientist teams on our radioactive material in a glass-like matrix. However, exjxxhtion, the other species were collected by divers radionuclides were also distributed in the rubble-filled along transects perpendicular to shore and adjacent to chimney, and the permanence of the vitrified residuals each of the three test sites and at Kiska. All specimens is unknown. As rainfall recharges the freshwater were tracked from field collection to their ultimate aquifer in the island's subsurface, radionuclides dis- analytic destination with chain of custody forms. Our solved in the flowing groundwater could be carried overall protocol was to collect enough sample through natural faults and fissures to the sea (DOE, material fiom each specific location to composite (at 2002a). The DOE'S groundwater model predicted that least five individuals) from a given site). Algae, fish breakthrough might occur any time fkom 10 to and birds were also collected at the same time (Burger 1,000 years after the blasts (DOE, 2002a), but their et al., submitted-a,b). risk assessment models predicted no current or future In the shipboard laboratory, all specimens were risk to humans (DOE, 2002b). Since it is already scanned with a handheld counter for gross alpha, several decades since the detonations, it is important gamma and beta. They were processed, measured to assess whether there has been any seepage and to (length, weight), cut into segments (octopus only), examine the concentrations of radionuclides in biota packaged and labelled. Samples were then immediate- as potential bioindicators for future biomonitoring. ly frozen for later analysis. Radionuclide analyses were CRESP's studies (Powers et al., 2005) refined these conducted on composites containing five or more estimates. (depending on size) individuals each. Most composites Kiska Island, the reference site, had similar were made up to 85 g, but some 1,000 g composites intertidal and benthic communities (Burger et al., in were analyzed for 72 h for 137~sto achieve appropri- press). It was occupied by the Japanese during World ate MDAs. For 1,000 g samples, many more War 11, and suffered intensive allied' bombing, but individuals were required per composite: Sea urchins never had any nuclear testing. (50-75 individuals), rock jingle (89-142 individuals), plate limpets (51-99 individuals), giant (109 2.2 Protocol individuals), and (1 15-229 individuals). All preparation and analytic work were performed in+, Under appropriate state collecting permits, invertebrates radio-clean laboratories, checked by daily wipe were collected hmthe intertidal and subtidal zones of samples (all below MDA). Samples were homoge- both Amchitka and Kiska Islands in a balanced design nized in a radio-clean and metal-clean laboratory at (where possible) from late June-July 2004. Species Rutgers University, and subsequently analyzed for collected were green sea urchin (Strongy10centrotu.s radionuclides at Vanderbilt University and Idaho polyacanthus), plate limpets (Tectura scurum), blue National Laboratory (INL). mussel (), giant Pacific octopus Our radionuclide analysis design was based on ( dopeini), giant chiton (Cryptochiton trophic group considerations, sample availability and stelleri), horse mussel (Mdiolus modiolus) and rock quantity (Table I). Detailed analytic and quality jingle (Podaiesmus macroschisma); all but the last assurance methods are published on the CRESP three are subsistence foods of the Unangan (Aleut) website www.cresp.org; Powers et al., 2005, 2006). peoples. Except for octopus, these were some of the We analyzed radioactive cesium ('37~s),iodine ('291), commonest species available, and they had a wide cobalt (60~o),europium (lS2~u),strontium eosr), distribution. These invertebrates represent different technetium (99~c),americium (241~m),plutonium nodes on the food chain, including grazers (chitons, (23sPu, 239,240 Pu), and uranium (234~,235~, 23&U, limpets, sea urchins), filter feeders (jingles, mussels), 238~). Analyses at Vanderbilt and Idaho National and predators (octopus). Further, they represent differ- Laboratory provided inter-laboratory validation Environ Monit Assess (2007) 128:32!&341 333

Table I Number of composites of invertebrates collected at Amchitka and Kiska analyzed for radionuclides

Species Cs 137 L129 Cod0 Eu-152 Sr-90 Alpha" Tc-99

Sea urchin 3 (4) 5 4 4 8 4 Rock jingle 3 (4) 4 4 4 4 2 1 3 Plate 2 Giant gumboot 1 Blue mussel 2 9 Horse mussel 8 Giant Pacific octopus 4 Shown for I3'cs are 1,000 g samples (100 g samples). All others were composites of 100 g or less. "Alpha analysis included the actinides "' Am, 238 h,239240 h,234 U, 235 U, 236 U, and 238 U.

(Powers et al., 2005). Gamma emitters (I3'cs, Is2~u, 6.25 Bq/kg for 100 g samples, and 0.184.36 Bqkg 60~o)were analyzed using gamma spectroscopy with for 1,000 g samples. high purity germanium detectors calibrated to the There were no values above the MDA for '29~,60~~, standard container geometry. 129~was analyzed by "EU, 90~r,99~c, and 238Pu,and these isotopes are not low energy photon measurement. The beta emitter discussed further. 90~rwas analyzed by its daughter decay product, yttrium-90 COY). Counts were adjusted for back- 3 Results ground counts, and the Minimum Detectable Activity (MDA) was * 2 SD background. The actinides 3.1 Radiocesium (uranium, plutonium, americium) were quantified using radiochemical techniques and alpha spectrosco- Only octopus haddetectable concentrations of '37~s,a11 py (average MDAs ranged from 0.052 for 241~mto other invertebrates, even with 1,000 g composites, 0.102 for 235~Bqlkg). All values are presented in Bql were below the MDA. Some composites had over 100 kg, wet weight, both in our samples and literature individuals (due to small body size). All four octopus data. Initially for gamma emitters we counted 100 g samples had detectable '37~sconcentrations (mean of samples for 24 h, but all results were below the MDA. 0.262 k 0.029 Bqkg, wet weight; maximum value of Thus to enhance sensitivity, we also analyzed 1,000 g 0.302 Bqlkg). Octopus were only collected at samples for 72 h. MDAs for '37~sranged from 5.57- Amchitka; none were found at Kiska.

Table II Comparison of actinide levels in invertebrates ------Source Rock jingle Blue mussel Horse mussel Chi square (P value)

Number of composites 2 1 9 8 Am-241 A 0.02 1 * 0.04 0.017 * 0.004 0.016 * 0.004 0.20 P < 0.90 Pu-239,240 A 0.024 * 0.012 0.019 * 0.004 0.022 * 0.011 0.49 P < 0.78 U-234 N 0.446 * 0.079 0.598 * 0.194 0.844 rt 0.804 5.69 P < 0.058 U-235 N 0.015 * 0.026 0.021 0.014 0.030 rt 0.048 1.28 P < 0.53 U-236 A (0.01 1) U-238 N 0.345 * 0.071 0.558 * 0.165 0.730 * 0.646 16.3 P < 0.003' Given are the means (A standard deviation, wet weight) in Bqkg with the values plus half the MDA for those below the MDA. Where there are very few values above the MDA for an isotope, the actual values are given in parenthesis. For source, A = anthropogenic, and N = natural. aThis difference is due to one high outlier, suggesting that this difference is not biologically significant.

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Table III Interisland comparison for actinides in rock jingles Isotope Range of reported Mean * SD Kruskal Wallis Number of Fisher Exact test values Chi Square detects (%) P value (from MDA to highest value)

Am-24 1 Amchitka Kiska Pu 239,240 Amchitka Kiska U-234 Amchitka Kiska U-235 Amchitka Kiska U-236 Amchitka Kiska U-238 Amchitka Kiska Given is mean * standard deviation (Bqkg, wet weight computed with values above the MDA and half the MDA for non-detects). Amchitka n = 15, Kiska n = 6 composites.

3.2 Actinides 4 Discussion

There were significant interspecific differences for 4.1 Interspecific and interisland comparisons 234~and 238~,both naturally occurring radionuclides (Table II). Horse mussels had significantly higher Interspecific differences in concentrations of contam- concentrations than the other species. There were no inants, including radionuclides, are usually due to differences in the anthropogenic radionuclides, per- differences in trophic concentration (Denton & haps due to their relatively low concentrations. Burdon-Jones, 1986; Jackson, 1991; Kasarnatsu & There were no interisland differences in any Ishikawa, 1997; Watms et al., 1998; Wiener and Spry, actinides for rock jingles, the species with the largest 1996; Burger et al., 2001), size and age (Lange, number of composites (Table Ill). Similarly, there Royals, & Connor, 1994; Burger et al., 2001; Pinho et were no interisland differences in actinides for blue al., 2002; Green & Knutzen, 2003), and habitat mussels (Table IV) or horse mussels (Table V). There (Burger et al., 2002). In general, concentrations are were also no interisland differences in the percent of higher in species that are larger, older, and in a higher composites above the MDA for rock jingles and trophic group. Trophic level relationships have also mussels. The concentrations are given by island for been reported for '37~s(Pentreath, 1973; Matishov & each species separately because these data will be Matishov, 2004), although Dietz et al. (2000) did not used as the baseline for long-term biomonitoring at find an increase in '37~sconcentrations with increas- Amchitka (Burger et al., 2006), and to allow other ing trophic level. At Amchitka, '37~sshowed a geographical comparisons. trophic group relationship only in that octopus had

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Table N Interisland comparison for actinides in blue mussels

Isotope Range of Mean =t SD Kmskal Wallis Number of Fisher Exact test reported values Chi Square detects (%) P value

Am-241 Amchitka Kiska (0.025) U-234 Amchitka -0.844 Kiska -0.949 U-235 Amchitka (0.045, 0.039) Kiska U-238 Amchitka -0.799 Kiska -0.844 Given is mean * standard deviation (Bqkg, wet weight (computed with values above the MDA and half the h4T-lA for non-detects). Amchitka n = 6 composites, Kiska n = 3 composites. Where there is only one value, it is given in parentheses. The full suite of actinides were analyzed, but they are not given if all were below the MDA. levels above the MDA, while other species did not. are the only isotopes with all composites above the Octopus was the only predatory invertebrate exam- MDA for blue mussel, horse mussel, and rock jingle. ined, the other species examined were grazers and For both isotopes, horse mussel had the highest filter-feeders (O'Clair, 1977). concentrations, and rock jingle had the lowest. We For the actinides, the only interspecific differences cannot account for this difference, since all three were in the naturally occurring 234~and 238~.These species are filter-feeders. It may be related to

Table V Interisland comparison for actinides in horse mussels

Isotope Range of Mean * SD Kruskal Wallis Number of Fisher Exact test repoIted Chi Square detects % P value values

Am-241 Amchitka Kiska Pu 239,240 Amchitka Kiska U-234 Amchitka Kiska U-235 Amchitka Kiska U-238 Amchitka Kiska Given is mean * standard deviation (Bqkg, wet weight (computed with values above the MDA and half the MDA for non-detects). Arnchitka n = 6, Kiska n = 2 composites.

a springer 226 Environ Monit Assess (20071 128:329-341

differential toxicokinetics (absorption, elimination United States (but not from Alaska). They drew several and storage) among the three species. conclusions: 1) 241Amand '37~sconcentrations were It is also useful to briefly compare the concen- higher along the West coast of the U.S. compared to the trations in the invertebrates with those for algae and East or Gulf coasts, 2) there were no significant fish (Burger et a]., unpublished data; Powers et al. locational differences for the other radionuclides, and 2005). There were no detectable concentrations of 3) there was a significant decline in radionuclide 137~sin algae, but there were interspecific differences concentrations in bivalves between the mid-1970s and in some radionuclides: UIva had the highest concen- the early 1990s. trations of 241~m,Alaria fistulosa had the highest concentrations of 2393240~~,and Fucus had the highest 4.2.1 Radiocesium concentrations of 234~,23%, and 238~.However, concentrations of all radionuclides were generally low Comparative datl for 137Cs yye available on some and near the for in In invertebrates (Table VI). Except for octopus, all contrast, there were significant differences in "'CS as in invertebrates at Amchitka were a function of species, but not location for top below the MDA; in the discussion below, we are thus predatory fish. Like the invertebrates, 2%J and 238~, the MDAs at Amchitka with the rePoneed isotopes that are primarily natural in origin, had the values or MDAs from elsewhere. The concentrations highest actinide detection rates in fish, and there were in the invertebrates at Amchi.a were similar to or no significant differences in mean concentrations below those from uncontaminated sites in the North- between Amchitka and Kiska. em Hemisphere, and were well below those from the Irish Sea. While the average concentration in non- 4.2 Geographical comparisons Irish Sea Northern Hemisphere sites (Table VI) is 0.03 Bqkg, some presumably uncontaminated sites Concentrations of radionuclides in seawater vary in have even higher concentrations. Concentrations for diffbent ; the seas with the highest concentra- mollusks frbm the Asia-Pacific regional seas averaged tions of key radionuclides are the Irish Sea (239,249~u, 0.1 Bqkg (Robison & Noshkin, 1999; Duran et al., ''~r, 137~s)and (13'cs, Livingston & 2004), although Ishikawa, Kagaya, and Saga (2004) Povinec, 2000). Similarly, concentrations of radionu- reported values of 0.03 Bqkg from the coast of Japan. clides vary in invertebrates. For example, Vale&-Silver From the , '37~sconcentrations and Lauenstein (1995) reported on concentrations of averaged 0.10 Bqkg generally (Sanchez-Cabeza & radionuclides in bivalves collected along the coastal Molero, 2000), but averaged 1.23 Bqkg from the

Table VI Com~arisonof '"CS levels in invertebrates Irish Seaa Other sitesb Amchitka (2004)'

Sea Urchin Mollusks Mean level 3.98 Range

Thermaikos Gulf in Greece (Catski & Florou, 2006). those we found at Arnchitka. Robison and Noshkin The variation, even within the Mediterranean, sug- (1999) reported mean 241~mvalues for mollusks at gests that site-specific information is essential, espe- Enewetak Atoll (0.020 * 0.005 Bqkg, wet weight) that cially for species that are used for subsistence or were similar to those we found at Amchitka. However, fisheries. the concentrations at Bikini Atoll were higher (0.32 & Although some studies report on crustaceans, as 0.29 Bqkg, Robison & Noshkin, 1999). Some of these well as mollusks (Duran et al., 2004), sea urchins are differences may be due to the year, since the Atoll data seldom examined (Matishov & Matishov, 2004). This span the period hm1972 to 1991, and to their use as may partly be due to technical difficulties. Digestion nuclear testing grounds (Robison & Noshkin, 1999). of sea urchins in this study ruined the platinum cruci- These analyses were based on sample sizes of 2-12 for bles, and we could not use the concentrations for all species of mollusks. actinides. The other difficulty with reported values by Robison and Noshkin (1999) reported mean group is that individual species cannot be compared 239,240~ufor shellfish from Bikini and Enewetak around the world; this seems to be particularly a prob- Atolls in Micronesia (0.032 * 0.024 Bqkg, wet lem with 'shellfish', rather than with algae or fish. weight), which was similar to the concentrations at There are relatively few data on contaminants in Amchitka. Skwarzec (1997) also reported mean octopus, mainly because they are difficult to capture concentrations of 239*2% from the Baltic Sea reliably, particularly from specific locations. Even for (0.022 i 0.001) that were very similar to those from metals, there are few data, and studies report concen- Amchitka. However, Shinohara (2004) reported mean trations from only 5 (Anderson, 2003) to 12 individuals 239,24% concentrations fbr shellfish (0.0036, maximum (Seixas, Bustamante, & Pierce, 2005). Gallelli, of 0.008 Bqkg), which were lower than Arnchitka, but Panatto, Perdelli, and Pellegrino (1997), however, similar to concentrations from the Mediterranean did measure 13'cs in two species of octopus from the (Sanchez-Cabeza & Molero, 2000). Both of the previous Ligurian Sea in northern Italy, and found means papers presented means without listing the species, the (*tandard deviation) of 14.8 * 10.9 and 10.6 & number of detects/nondetects, or the MDAs. It is thus 10.4 Bqkg in 1987, and 2.5 & 2.1 and 4.8 k 4.3 Bqkg difficult to evaluate whether many values were above in 1988. This may relate to time since the Chernobyl detection limits. This limits their use for comparative accident (April 26, 1986), and it is important to have purposes, and for selection of bioindicators. Further, more recent data. The mean 13'cs concentrations in computing the dose to non-human or human consumers octopus from Amchitka were 0.26 + 0.029 Bq/kg, of shellfish fkom data without such parameters is much lower than those from the Ligurian Sea. difficult. The significance of exposure assessments for Because of their ability to concentrate '37~s,Gallelli non-human biota based on empirical data with such data et al. (1997) suggested that they would be a good gaps may lead to faulty risk characterization (Avila et bioindicator. Yamada et al. (1999) examined two al., 2004). This lack of species-specific information for species of octopus fiom the Japanese coast and found shellfish is even more problematic when computing low concentrations of I3'cs (mean of 0.075 Bqkg for human dose, which must relate directly to consumption two ). patterns for different species (or types) of shellfish. Few studies report the concentrations of the natu- 4.2.2 Actinides rally occurring actinides. However, Rollo, Camplin, Allington, and Young (1992) analyzed a range of There are also few comparative data on actinides for invertebrates and fish from the marine environment of invertebrates, and often the data are presented only as the United Kingdom. Mean concentrations of 234~in concentration factors, and not as the concentrations shellfish ranged from 1.4-5.6 Bqkg (wet weight), (needed for comparisons among regions). Sanchez- 235~ranged from 0.027-0.19 Bqkg, and 238~ranged Cabeza and Molero (2000) reported 241~rnconcentra- from 1.2-5.5 Bqkg (Rollo et al., 1992). The concen- tions of 0.004 Bqkg in mussels hmthe Mediterranean trations at Amchitka were all well below these Sea, and Mmo, Fiori, Jia, and Chiantore (2000) concentrations, but higher than those fiom the coast reported 24'~mconcentrations of 0.002 Bqkg in of Japan (0.20 Bqkg 238~,Ishikawa et al., 2004). The mussels hmthe Antarctic; both were much lower than concentrations of 238~in bivalves from the Baltic Sea

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(average 0.69 Bqkg, Skwarzec, 1997), were similar are better than others. That is, the species that accu- to those in bivalves from Amchitka. However, the mulate the most, even in a region of relatively low concentrations of 23%J from the Mediterranean Sea concentrations, would be the best bioindicators. (mean of 0.0002 Bqkg, Sanchez-Cabeza & Molero, Finally, for invertebratesto be usefbl as bioindicators, 2000), and Antarctic (mean of 0.001, Marzano et al., concentrations must be attributable to individual spe- 2000), were well below those found at Amchitka. In cies. For example, there are thousands of species of sharp contrast, concentrations of 238~from the benthic organism in the seas (Matishov & Matishov, eastern Black Sea averaged 35 Bqkg, wet weight 2004). Thus, there is a clear need for authors to report (Topcuoglu, Ergul, Baysal, Olmez, & Kut, 2003). concentrations by species (along with MDAs and Although uranium formed at the time of the Earth's percent of samples above the MDA), and then group creation about 4.7 billion years ago, it is not them by 'shellfish' if this is necessary for other uniformly distributed over the surface. Concentrations purposes. While it is helpful to lump many species tend to be higher in rocks of volcanic origin, for into a 'shellfish' category when examining overall example, than in sedimentary rocks (USGS, 2006). tmphic relationships (primary producers, herbivores, Thus the contribution of surface erosion to uranium predators), it is not when examining specific risk to the content of the sea would be higher in areas with individual species themselves, or to predators that eat relatively rich soils. them. People do not eat shellfish, they eat mussels, , or . Risk can only be determined using 4.3 Use of invertebrates as bioindicators contaminant levels in specific shellfish, and consump- tion rates of those individual species. That is, assessors Many invertebrates accumulate contaminants, such as determine the risk from consuming mussels or clams. radionuclides, because they are sedentary or not very mobile, are benthic, and graze or filter feed. They are Acknow1edgements We thank the many people who contrib- ideal indicators because they can accumulate radio- uted to the development and execution of CRESP's Amchitka . nuclides many times above the concentrations in Geophysical and Biological Project, especially C. W. Powers seawater (Matishov & Matishov, 2004). Where con- and D. Kosson. We also thank the following for help centrations in seawater and sediment are very low, throughout the project, D. Volz, B, Friedlander, Q. Yyas, H. Mayer, D. Barnes, L. Duffy, A. Morkill, R. Patrick, D. Rogers, however, all analyses might well be below the MDA, D. Dasher, and the people of the villages of Unalaska, Nikolski, as occurred in this study for several radionuclides Atka, and Adak in the Aleutians. Technical help was provided (129~,60~~, 52~~, *~r, 99~c,238~~), and even for by S. Bwke, C. Jeitner, D. Snigaroff, R. Snigaroff, T. Stamm, '37~s(except for the predatory octopus). Further, in S. Harper, M. Hoberg, H. Chenelot, R. Patrick, M. Donio, S. Shukla, and C. Dixon. We thank the entire crew of the Ocean order to achieve low enough detection concentrations Explorer, Captain Ray Haddon, mate Glenn Jahnke, cook Don of '37~sin octopus, we had to use 1,000 g samples, Dela CIUZ,and Bill Dixon, Joao Do Mar, and Walter Pestka, for counted for 72 h. While it is not difficult to obtain making our field work possible and pleasant, and for bringing enough material from octopus for large composites, it us safely back to port. This research was funded by the Consortium for Risk Evaluation with Stakeholder Participation is more dificult for smaller species, such as limpets, (CRESP) through the Department of Energy (DE-FG 26-00NT mussels, and sea urchins. And all of these were con- 40938), by Wildlife Trust, and by NIEHS ESO 5022. The sidered delicacies by the Aleut team members. These results, conclusions and interpretations reported herein are the are commonly used subsistence foods (APIA, 2002; sole responsibility of the authors, and should not in any way be interpreted as representing the views of the funding agencies: Patrick, 2002; Hamrick & Smith, 2003), especially if Aleuts are stranded overnight during hunting forays or when they first land on beaches to set up temporary camps. References Invertebrates seem to be particularly usefbl for actinides, however, where small sample sizes can be Aarkrog, A. (2003). Inputs of anthropogenic radionuclides into used. All of the composites were above the MDA for the the world ocean. Deep-Sea Research, SO, 2597-2606. Amundsen, I., Iosjpe, M., Reistad, O., Lind, B., Gussgaard, K., naturally occurring 234~and 238~.Since there were Strand, P., et al. (2002). The accidental sinking of the interspecific differences for these isotopes (horse nuclear submarine, the Kursk: Monitoring of the radioac- mussels had the highest concentrations), some species tivity and the preliminary assessment of the potential

@ Springer Environ Monit Assess (2007) 128:329-341 - impact of radioactive releases. Marine Pollution Bulletin, radionuclide concentrations in a bio-indicator Mytilus 44,459-468. galloprovincialis from the French Meditenanean coast. Anderson, R. C. (2003). A preliminary report on bioaccumu- Science of the Total Environment, 237/238, 93-103. lation in (Enteroctopus dofleini). Proceed. Cooper, L. W., Beasley, T. M., Zhao, X. L., Doto, C., GeorgiaPuget Sound Res. Conz, 2, 1-5. Vinogradova, K. L., & Dunton, K. H. (1998). Iodine-129 APIA (Aleutian Pribilof Islands Association) (2002). Atka and plutonium isotopes in arctic kelp as historical traditional food sampling survey. Anchorage, Alabama: indicators of transpolt of nuclear fuel-reprocessing wastes APIA. from mid-to-high latitudes in the . Marine Aumento, F., Donne K. L., & Eroe, K. (2005). Transuranium Biology, 131, 391-399. radionuclide pollution in the waters of the La Maddalena Dasher, D., Hanson, W., Read, S., Faller, S., Farmer, D., Efurd, National Marine Park. Journal of Environmental Radio- W., et al. (2002). An assessment of the reported leakage of activity, 82, 81-93. anthropogenic radionuclides fiom the underground nuclear Avila, R., Beresford, N. A., Aguero, A., Broed, R., Bmwn, J., test sites at Amchitka Island, Alaska, USA to the surface Iospie, M., et al. (2004). Study of the uncertainty in environment. Journal of Environmental Radioactivity, 60, estimation of the exposure of non-human biota to ionizing 165-187. radiation. Journal of Radiological Protection, 24, 105-1 22. Denton, G. R. W., & Burdon-Jones, C. (1986). Trace metals in Baeza, A., Miro, C., Paniagua, J. M., Navarro, E., Rodriguez, fish from the Great Barrier Reef. Marine Pollution Bulletin, M. J., & Sanchez, F. (1994). Natural and artificial 17,201-209. radioactivity levels in Livingston Island (Antarctic Department of Energy (DOE) (2000). United States Nuclear regions). Bulletin of Environmental contamination and Tests July 1945 through September 1992, Nevada Oper- Toxicology 52, 117-124. ations Office, Las Vegas, Nevada (DOEN-209). BNFL (2004). Discharges and monitoring of the environment Department of Energy (DOE) (2002a). Modeling Groundwater in the UK, Annual report. httjx/iwww.bnfl.com/dischar Flow and Transport of Radionuclides at Amchitka Island's 002.htm. Underground Nuclear Tests: Milrow, Long Shot, and Bolo,, ... ,. ,,,O). Radioactivity assessment of the Black Cannikan. Nevada Operations Office, Las Vegas, Nevada Sea with special emphasize on the Romanian sector. (DOEN-I 1508-5 1). Radiol. Impact Assess. SE Mediterranean, 2, 61-74. Department of Energy (DOE) (2002b). Screening Risk Assess- Burger, J., Gaines, K. F., Boring, C. S., Stephens Jr., W. L., ment for Possible Radionuclides in the Amchitka Marine Snodgmss, J., & Gochfeld, M. (2001). Mercu~~and selenium Environment. Nevada Operations Ofice, Las Vegas, in fish Grom the Savannah River. Species, trophic level, and Nevada @OE/NV-857). locational differences. Environmental Research, 87, 1% 1 18. Dietz, R., Riget, F., Cleemann, M., Aarkrog, A., Johansen, P., Burger, J., Gaines, K. F., Boring, C. S., Stephens, W. L., & Hansen, J. C. (2000). Comparison of contaminants fiom Snodgrass, J., Dixon, C., et al. (2002). Metal levels in fish different trophic levels and ecosystems. Science of the from the Savannah River: Potential hazards to fish and Total Environment, 245, 221-23 1. other receptors. Environmental Research, 89, 85-87. Duran, E. B., Povinec, P. P., Fowler, S. W., Airey, P. L., & Burger, J., Gochfeld, M., Kosson, D. S., & Powers, C. W. (2006). Hong, G. H. (2004). I3'cs and 239,240~~levels in the Asia- Biomonitoring for ecosystem and human health protection Pacific regional seas. Journal of Environmental Radioac- at Amchitka Island. Consortium for Risk Evaluation with tivity, 76, 13S160. Stakeholder Participation. Piscataway, New Jersey. Eichelberger, J. C., Freymueller, J., Hill, G., & Patrick, M. Burger, J., Jewett, S., Gochfeld, M., Hoberg, M., Harper, S., (2002). Nuclear stewardship: Lessons from a not-so- Chenelot, H., et al. (in press). Can biota sampling for remote island. Geotimes, 47, 20-23. environmental monitoring be used to characterize benthic Faller, S. H., & Farmer, D. E. (1998). Long-term Hydrological communities in the Aleutians? Science of the Total Monitoring Program: Amchitka, Alaska. Washington, Environment. District of Columbia: U.S. Environmental Protection Catski, V. A., & Florou, H. (2006). Study on the behavior of Agency (EPA-402-R-98-002). heavy metals Cu, Cr, Ni, Zn, Fe, Mn and '"CS in an Farrington, J. W., Davis, A. C., Tripps, B. W., Phelps, D. K., & estuarine ecosystem using Mpilus galloprovincialis as a Galloway, W. B. (1987). Mussel watch: Measurements of bioindicator species: The case of Thmaikos gulf, Greece. chemical pollutants in bivalves as one indicator of coastal Journal of Environmental Radioactivity, 86, 3 1- 44. environmental quality, pp 125-139 in New approaches to CEFAS (Center for Environment, Fisheries and Aquiculture monitoring aquatic ecosystems, Am. Soc. Testing and Science) (2003). Radioactivity in food and the environ- materials, Philadelphia, Pennsylvania. ment. Environment Agency, Environment and Heritage Fisher, N. S., Fowler, S. W., Boisson, F., Carroll, J., Rissanen, Service; Food Standards Agency; Scottish Environment K., Salbu, B., et al. (1999). Radionuclide bioconcentra- Protection Agency (RIFE 8). tion factors and sediment partition coefficients in Arctic CEFAS (Center for Environment, Fisheries and Aquiculture Seas subject to contamination from dumped nuclear Science) (2004). Radioactivity in food and the environ- wastes. Environmental Science and Technology. 33, ment. Environment Agency, Environment and Heritage 1979-1 982. Service; Food Standards Agency; Scottish Environment Gallelli, G., Panatto, D., Perdelli, F., & Pellegrino, C. (1997). Protection Agency (RIFE 9). Long-term decline of radiocesium concentration in sea- Charmasson, S., Barker, E., Calmet, D., Pmchon S. S., & food from the Ligurian Sea (Northern Italy) after Cher- Thebault, H. (1999). Long-term variations of man-made nobyl. Science of the Total Environment, 196, 163-170.

Q Springer Environ Monit Assess (2007) 128:32%341

Green, N. W. & Knutzen, J. (2003). Organohalogens and metals Matishov, G. G., Matishov, D. G., Anisimova, N. A., in marine fish and mussels and some relationships to Dzhenyuk, S. L., & Zuev, A. N. (2001). Radiation biological variables at reference localities in Norway. conditions of the environment and biota on the Murmansk Marine Pollution Bulletin, 46, 362-377. Bank in the area of the sunken Kursk nuclear submarine. Hamrick, K, & Smith, J. (2003). Subsistence food use in Oecologia, 41,853-860. Unalaska and Nikolski. Anchorage, Alabama: Aleutian Memtt, M. L., & Fuller R. G. (Eds.). (1977). The Environment Pribilof Island Association. of Amchitka Island, Alaska, US., Technical Information Hong Kong Observato~y. (2003). Environmental radiation Center, Energy Research and Development Administra- monitoring in Hong Kong. Technical Report, 22. tion, Washington, District of Columbia (Report NVO-79). Hung, T. C., Huang, C. C., & Shao, K T. (1998). Ecological Moscati, A. F., & Erdmann, R. C. (1974). Possible effects of survey of coastal water adjacent to nuclear power plants in ionizing radiation upon and some implications Taiwan. Chmisby and Ecology, 15, 129-142. of postulated accidental releases of radioactivity. Nuclear IAEA (1999). Inventory of radioactive waste disposal at sea. Technology, 22, 184-190. IAEA Techdoc Ser: No. 1105, 121 pp. National Research Council (NRC) (1996). The Bering Sea Ishikawa, Y., Kagaya, H., & Saga, K. (2004). Biomagnification ecosystem. Washington, District of Columbia: National of '~e,234~h, and "'~a in marine organisms near the Academy. no&ern Pacific coast of Japan. Journal of Environmental Noms, R. S., & Arkin, W. M. (1998). NRDC nuclear notebook Radioactivitv. 76, 103- 112. known nuclear tests worldwide, 1945-1998. Bull. Atomic Jacob, K. (1984):~&ates of long-term probabilities for future Sci. November/December. great earthquakes in the Aleutians. Geophysical Research O'Clair, C. E. (1977). in rocky inter- Letters, 11, 295-298. tidal communities. In M. L. Memtt & R. G. Fuller Jackson, T. A. (1991). Biological and environmental control of (Eds.), The environment of Amchitka Island, Alaska, US. mercury accumulation by fish in lakes and reservoirs of (pp 39549). Washington, District of Columbia: Techni- Northern Manitoba, Canada. Canadian Journal of Fisher- cal Information Center, Energy Research and Develop- ies and Aquatic Sciences, 48, 2449-2470. ment Administration (Report NVO-79). JCAC (Japan Chemical Analysis Center) (2003). Radioactivity O'Neill, D. T. (1994). The firecracker boys. New York, New survey data in Japan: Environmental and dietary materi- York: St. Martin. ab. Rep. No. 138. JCAC, Chiba, Japan. Page, R. A., Biswas, N. N., Lahr, J. C., & Pulpan, H. (1991). JCAC (Japan Chemical Analysis Center) (2004). Radioactivity Seismicity of continental Alaska. In D. B. Slemmons, E. survey data in Japan: Environmental and dietary materi- R. Engldahl, M. D. Zoback, & D. D. Blackwell (Eds.), als. Rep. No. 139. JCAC, Chiba, Japan., Neotectonics of North America (pp 47-68). Boulder, Jewett, S. C. (2002). Radionuclide contamination in nearshore Colorado: Geological Society of America. habitats around Amchitka Island, Alaska. In Proceedings Patrick, R. (2002). How local Alaska native communities view of the Amchitka Long-term Stewardship Workshop, the Amchitka issue. In Proceedings of the Arnchitka long- CRESPRTniversity of Alaska. Fairbanks, Alaska (held term stewardship workshop, CRESPiUniversity of Alaska. 12-14 February 2002). Fairbanks, Alaska (held 12-14 February 2002). Kasamatsu, F., & Ishikawa, Y. (1997). Natural variation of Pentreath, R. J. (1973). The roles of food and water in the radionuclidesuper(1 37)Cs concentration inmarine organisms accumulation of radionuclides by marine teleost and with special reference to the effect of food habits and trophic elasmobranch fish. In Symposium on the Interactions of level. Marine Ecology. Progress Series, 160, 1W120. radioactive contaminants with the constituents of the Kohlhoff, D. W. (2002). Amchitka and the bomb: Nuclear marine environment (pp 421-436). Seattle, Washington. testing in Alaska. Seattle, Washington: University of Pinho, A. P., Guimaraes, J. R. D., Marins, A. S., Costa, P. A. S., Washington. Olavo, G., & Valentin, J. (2002). Total mercury in muscle Lange, T. R., Royals, H. E., & Connor, L. L. (1994). Mercury tissue of five shark species from Brazilian offshore waters: accumulation in largemouth bass (Micropterussalmoides) Effects of feeding habit, sex, and length. Journal of in a Florida Lake. Archives of Environmental Contamina- Environmental Research, 89, 250-258. tion and Toxicology. 27, 466 - 471. Poon, C. B., & Au, S. M. (2002). Modelling the super (127) Cs Livingston H. D., & Povinec, P. P. (2000). Anthropogenic marine ingestion dose from consumption of marine fish in Hong radioactivity. Ocw & Coastal Management, 43, 689-7 12. Kong. Radiation Protection Dosimetry, 98, 199-209. Lystsov, V., Murzin, N., & Nezhdanov, G. (1999). Assessment Powers, C. W., Burger, J., Kosson, D., Gochfeld, M., & Barnes, of the risk created by the objects with spent nuclear fuel D. (Eds). (2005). Amchitka independent science assess- dumped in the Kara Sea and instrument all possibilities of ment: biological and geophysical aspects of potential the early warning about radionuclide discharges from radionuclide exposure in the Amchitka marine environ- these objects. Sympos. Mar. PoN. 634-635, Monaco. ment. Consortium for risk evaluation with stakeholder Marzano, F. N., Fiori, F., Jia, G., & Chiantore, M. (2000). participation. Piscataway, New Jersey. Anthropogenic radionuclides bioaccumulation in Antarctic Powers, C. W., Burger, J., Kosson, D., & Gochfeld, M. (2006). marine fauna and its ecological relevance. Polar Biology. 23, Additional radiological data for bioindicator selection. 753-758. Consortium for risk evaluation with stakeholder partici- Matishov, D. G., & Matishov, G. G. (2004). Radioecology in pation. Piscataway, New Jersey. Northern European Seas. Berlin Heidelberg New York: Robbins, A., Makhijani, A., & Yih, K. (1991). Radioactive Springer. heaven and earth - The health and environmental effects

Springer Environ Monit Assess (2007) 128:329-341

of nuclear weapon testing in, on and above the earth. New Reprocessing Plant. Journal of Environmental Radioadvi@, York, New York: Apex. 72,299-322. Robison, W. L., & Noshkin, V. E. (1999). Radionuclide Skwanec, B. (1997). Polonium, uranium, and plutonium in the characterization and associated dose from long-lived southern Baltic Sea. Ambio, 26, 113-1 17. radionuclides in close-in fallout delivered to the marine Togawa, O., Povinec, P. P., & Pettersson, H. B. L. (1999). environment at Bikini and Enewetalc Atolls. Science of the Collective dose estimates by the marine food pathway 60m Total Environment, 237, 3 11-327. liquid radioactive wastes dumped in the Sea of Japan. Rollo, S. F. N., Camplin, W. C., Allington, D. J., & Young, A. Science of the Total Environment, 237-238,241-248. K. (1992). Natural radionuclides in the UK marine Topcuoglu, S., Ergul, H. A., Baysal, A., Olmez, E., & Kut, D. environment. Rad. Prot. Dos., 45, 203-209. (2003). Determination of radionuclide and heavy metal RPII (2003). Radioactivity monitoring of the Irish marine concentrations in biota and sediment samples from Pazar environment 2000 and 2001. The Radiological Protection and Rize stations in the eastern Black Sea. Fresenius Institute of Ireland. RPI-03/3. Environmental Bulletin, 12, 695-699. RPII (2004). Radioactivity monitoring of the Irish marine UNSCEAR (2000). Sources and efects of ionizing radiation. environment 2002. The Radiological Protection Institute of United Nations Scientific Committee on the Effects of Ireland. RPI-03f3. http://www.rpii.ie/radiatiod~2002/ Atomic Radiation, 2000 Report to the General Assembly, start.htmi. United Nations, New York, pp. 158-172. SanchezCabem, J. A., & Molero, J. (2000). Plutonium, americi- Valette-Silver, N. J., & Lauenstein, G. G. (1995). Radionuclide um and radiocesium in the marine environment close to the concentrations in bivalves collected along the coastal Vandellos I nuclear power plant before decommissioning. United States. Marine Pollution Bulletin, 30, 320-331. Journal of Environmental Radioactivi& 51, 21 1-228. USGS (United States Geological Survey) (2006). The geology Seymour, A. H., & Nelson, V. A. (1977). Radionuclides in air, of radon. Washington D.C.: U.S. Geological Survey water, and biota. In M. L. Menitt & R. G. Fuller (Eds.), The (accessed February 2, 2006). hnp://energy.a.usgs.gov/ environment of Amchitka Island, Alaska @p 579-613). radodgeoradod3.hbnl. Washington, District of Columbia: Technical Information Watras, C. J., Back, R. C., Halvorsen, S., Hudson, R. J. M., Center, Energy Research and Development Administration Morrison, K. A., & Wente, S. P. (1998). Bioaccumulation (Report TID-267 12). of mercury in pelagic freshwater food webs. Science of the Seixas, S., Bustamante, P., & Pierce, G. (2005). Accumulation Total Environment, 219, 183-208. of mercury in the tissues of the (Octopus Wiener, J. G., & Spry, D. J. (1996). Toxicological significance of vulgaris (L.) in two localities on the Portuguese coast. mercury in freshwater fish. In W. N. Beyer, G. H. Heins, & Science of the Total Environment, 340, 1 13-122. A. W. Redmon-Norwood (Eds.), Environmental contami- Shenber, M. A., Elshamis, E. E., Ekikli, A. T., & Elayan, M. nants in wildlife (pp 297-339). Boca Raton, Florida: N. (1999). Radiocaesium-137 in some marine species in Lewis coastal zone of Libya (Sirt Gulf). Symp. Mar Poll. pp. Yamada, M., Aono, T., & Hirano, S. (1999). 239,249~~and I3'cs 56&569. Oct 5-9, Monaco. concentrations in fish, , crustaceans, shellfish, Shinohara, K. (2004). Assessment of radiological effects on the and algae collected around the Japanese coast in the early regional environment due to the operation of the Tokai 1990s. Science of the Total Environment, 239, 13 1-142.

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