1. Scott W. Fowler School of Marine and Atmospheric Sciences Stony Brook University Stony Brook, NY, USA Brief Introduction to Marine Radioecology with Emphasison Bioaccumulation in Marine Organisms Brief Introduction to Marine Radioecology with Emphasis on Bioaccumulation in Marine Organisms

2. What is Marine Radioecology? -A specialized discipline of marine ecology which studies how radioactive substances interact with the marine environment, and how different mechanisms and processes affect radionuclide migration in the marine food chain and ecosystem. - Can include aspects of field sampling, designed field and laboratory radiotracer experiments, and the development of predictive simulation models. - Requires basic knowledge of biology, ecology, chemistry, geology, biogeochemistry, oceanography, and radiation protection.

3. Biogeochemical transfer and transport pathways of radionuclides in the marine environment

4. How Are Radionuclides Taken Up By Marine Organisms? From water: - Adsorption to Cell/Body Surfaces - Absorption across Cell/Body surfaces - Combination of Both Sorptive Processes From Food: - Ingestion of Contaminated Prey Organisms followed by Assimilation of Radionuclide across the Gut Wall From Sediment: - Ingestion of Contaminated Sediments - Adsorption and/or Absorption of the Soluble Radionuclide present in Pore Water between the Sediment Grains

5. Main Factors Affecting Bioaccumulation of Radionuclides Environmental: Temperature Salinity Trace Metal Competition Oxidation State (chemical form) Organic Complexation Exposure Time Biological: Age Size Sex Reproductive State Physiology & Metabolism Food Type Feeding Mode Ingestion Rate Filtering Rate Assimilation Efficiency External Tissue Composition

6. Concentration Factor Ratio of radionuclide concentration in organism to radionuclide concentration in ambient sea water Assumptions: - Generally refers to equilibrium situation - Uptake is from soluble form in water Calculation: CF = Bq g -1 wet weight of organism Bq g -1 sea water Uses: - Compare relative bioavailability of different radionuclides to a given organism - Compare ability of different organisms to accumulate a a given radionuclide - Through models we can predict the resultant concentration in an organism if the concentration in sea water is known - To identify potential “bioindicator organisms” for radionuclides

7. Uptake of 241 Am and 134 Cs from sea water by the scallop, Pecten maximus (n=9). From Metian et al. 2011

8. Species dependent uptake of plutonium from sea water by various marine organisms (from Fowler, 1983) Radiotracer experiments

9. Uptake from sea water of reduced (III+IV) and oxidized (V+VI) forms of plutonium by clams (Aston & Fowler, 1984)

10. Effect of Temperature on Uptake of 60 Co, 241 Am and 134 Cs from Water by Brown Macroalgae (Fucus vesiculosus) 12 o C ( ○ ) 2 o C ( ● )

11. ← 22 o C ( ∆ ) ← 13 o C ( X ) ← 8 o C ( ● ) Effect of Temperature on Uptake of 109 Cd from Water by Benthic Shrimp (Lysmata) and Mussels (Mytilus)

12. Organism 137 Cs 239+240 Pu 241 Am 210 Po Macroalgae 15 – 33, 12 - 20290, 770, 400080001000 - 7000 Phytoplankton 20100000 2800 - 7400 Zooplankton 14, 174000 19000 - 61000 Decapod crustaceans 11, 26 ± 107514510000 - 150000 Benthic molluscs 7110 – 200200, 330, 55015000 - 69000 Cephalopods 7, 1050, 6535, 1009000 - 30000 Echinoderms 3, 62 ± 407, 310, 55026000, 28000- Polychaetes 6130, 200100017000 - 23000 Coelenterates 1.6 – 3.6-1.2 - 12- Teleost fish 23, 52 ± 4 (14 – 133), 59 ± 24 100, 3501002000 - 9000 * Concentration factor = Bq g -1 organism wet weight / Bq g -1 sea water Means (ranges) of Concentration Factors* of selected radionuclides in different taxonomic groups based primarily on field data

13. Size Spectrum of Living Marine Biogenic Particles ↑ ↑ 1 μm ----------------------------------- 10 cm Within the 0.4 – 10 μm size range, there are ~ 10 7 particles ml -1 in top 50 m, and > 95% are non-living organics

14. Relationship of log volume concentration factor (VCF) for transuranic elements with log surface:volume ratio in marine palankton. ( ● ) Am, ( ○ ) Pu, ( ∆ ) Cf, ( □ ) Cm, and ( ▲ ) Am in appendicularians (from Fisher & Fowler, 1987)

15. Uptake of 134 Cs from sea water by flatfish (plaice) of different weights (from Pentreath, 1975)

16. Loss of 241 Am and 134 Cs from scallops (Pecten maximus; n=9) following 7 day uptake from sea water (From Metian et al. 2011)

17. Depuration of plutonium by clams (Venerupis) and worms (Hermione) after 22 days exposure in labelled sea water (Aston & Fowler, 1984)

18. Accumulation of Plutonium and Americium from Seawater by Octopus followed by Long-term Depuration in Uncontaminated Sea Water Curve (1): Loss of Pu and Am after 10 day exposure Curve (2): Loss of Am after 22 day exposure Octopus vulgaris

19. Loss of 241 Am from contaminated euphausiid zooplankton following uptake from water - Dashed lines denote molting of each individual - Dashed lines denote molting of each individual - Molts contained 96 ± 10% of the Am body burden - Molts contained 96 ± 10% of the Am body burden

20. 241 Am transfer factors (TF) in worms (Hermione) and clams (Venerupis) exposed to radio-labelled NE Atlantic and NW Pacific sediments Worms (Pacific) Worms (Atlantic) Clams (Pacific) Clams (Atlantic) TF = Bq g -1 wet weight of organism Bq g -1 wet sediment

21. Uptake of plutonium from labelled NE Atlantic sediments by clams and polychaetes. Data represent 6 individuals (from Aston & Fowler, 1984)

22. OrganismUptake (days) 239+240 Pu 241 Am 137 Cs 60 Co Worms Nereis 11-500.00160.00090.20.06 Arenicola140.0020.003 Clams Venerupis 40-500.0060.004-0.02 Scrobicularia140.010.008 Isopod Cirolana 40-500.006-0.032 Amphipod Corophium 140.100.11 Transfer factors* of radionuclides accumulated from contaminated sediments * Transfer factor = Bq g -1 organism wet weight / Bq g -1 wet sediment

23. Loss of Plutonium after Single Ingestion of Contaminated Worms by 6 Individual Crabs (Carcinus maenas) Pu Assimilation Efficiencies (AE) were estimated by resolving the different components of the loss curves by standard mathematical methods used in radioecology. AE is then determined graphically by extrapolation of the long-lived loss component (solid line) to time zero Rapid loss during first 2-4 days due to gut clearance of unassimilated Pu → AE = 20 – 60% of ingested Pu 45 – 85% is in hepatopancreas 8 - 43% associated with shell 5 -10% is in muscle and gill

24. OrganismFood type 137 Cs 239+240 Pu 241 Am 60 Co 110m Ag 210 Po Zooplankton Cope/Euphausiid Phytopl Artemia -0.8 – 10.9 – 1014 - 458 – 1920 - 55 Decapod Crustaceans Artemia Worms Mussels -10 - 608 - 58~ 9935 Bivalve Molluscs Phytopl3 - 40.90.6 - 388 - 833 - 4917 CephalopodsCrabs Mussels 23 - 29-31 - 60--- EchinodermsMussels Clam 8270 - 9026 - ~10022 - 7334 – 69- Teleost fishShrimp Clam Fish 42 - 950.1 – 10.7 – 624 – 185 Assimilation efficiencies ( AE ) of key anthropogenic and natural radionuclides in selected marine taxa determined by laboratory radiotracer experiments

25. Organism/Tissues*(mSv y -1 ) Phytoplankton0.30 – 3.2 Mixed Zooplankton2.4 – 16.6 Benthic polychaetes2 - 38 Benthic isopods3.1 – 4.7 Benthic amphipod3.3 Benthic shrimp5.1 Bivalve molluscs2.9 – 13.5 Cephalopods3.2 - 11 Mesopelagic carid shrimp3.6 Mesopelagic penaeid shrimp49 Mesopelagic penaeid hepatopancreas580- 3900 Pelagic Fish muscle1 - 5.9 Fish liver3 - 295 Fish pyloric caecum7 - 2130 Fish gonad3 - 171 Dose-equivalent rates (mSv y -1 ) based on 210 Po Dose-equivalent rates (mSv y -1 ) based on 210 Po concentrations reported for various species and tissues concentrations reported for various species and tissues * 1 mSv y -1 = 100 mrem y -1

26. Tissue * Food % Total Pu ** Seawater † NW Mediterranean, Monaco † † La Hague, France Body wall (Epidermis) (Skeleton) 19.498.0 (65.7) (32.3) 95.495.1 Pyloric caeca74.31.43.53.4 Gut6.30.60.90.6 Gonad--0.21.0 * 4 individuals fed for 0.5 day and dissected after 1 – 3 months ** 10 individuals exposed in labeled seawater for 10 days and then dissected † 100 individuals dissected after lifetime exposure to Pu from fallout † † 20 individuals dissected after lifetime exposure to Pu from fallout & released nuclear wastes Relative distribution of plutonium in tissues of starfish after prolonged exposure from radio-labeled seawater and food under laboratory conditions, and those living in the natural environment

27. 137 Cs concentration (dry weight) in different size classes of male and female European Hake (from Harmelin-Vivien et al. 2012) Numbers in bars = no. of individuals analyzed. Significance of male-female difference: ns = not significant, * = p < 0.05, ** = p < 0.01

28. Chernobyl radionuclides in sinking particles (Bq g -1 dry) collected at 200m depth in a 2200m water column in the NW Mediterranean Sea

29. Zooplankton Fecal Pellet Types Salps Pteropods (Gymnosomata and Thecosomata) Euphausiids Copepods

30. Organism 239+240 Pu 241 Am 210 Po 137 Cs 134 Cs Phytoplankton 1.0, 0.350.052, 0.2221 – 61-- Copepods Fecal pellets 0.05 – 0.48 1.2, 3.4 0.022, 0.12 1.0, 2.7 126 617 *34 ± 7 *6300 ± 1000 *22 ± 6 *3400 ± 600 Euphausiids Fecal Pellets Molts 0.015 3.6 0.18 (90%) ------ 40.7 648 – 1000 13.3 (2.5%) ------ ------ Salps Fecal pellets - 8.9 - 5.0 260 583 - 750 ---- ---- † Japanese Copepods (Pre – Fukushima) ---0.42 ± 0.15- **Japanese Copepods (Post – Fukushima) ---14.8 ± 14.9 Max = 56 17.7 ± 13.7 Max = 46 Concentrations of selected radionuclides (Bq kg-1 dry) in zooplankton and sinking particulate products released into the water column ( ) = Percent of euphausiid whole body radionuclide concentration contained in the molt * Samples are Chernobyl fallout-enriched, Fowler et al, 1987 † Tateda, 1998 ** Buesseler et al, 2012

31. 239+240 Pu concentration in bivalve soft parts collected at Thule, Greenland in 1968, 1970 and 1974 as a function of the distance from the point of impact of the B-52 nuclear accident (source = ~ 1TBq) r 2 = Corr. Coeff. between observed data and values calculated from the exponential equations *** 0.001 level of significance

32. 239+240 Pu concentration (pCi kg -1 wet weight starfish, molluscs, shrimp; pCi g -1 sediment and worms) in a contaminated Thule ecosystem as a function of distance from the point of impact of the nuclear accident 239+240 Pu concentration (pCi kg -1 wet weight starfish, molluscs, shrimp; pCi g -1 sediment and worms ) in a contaminated Thule ecosystem as a function of distance from the point of impact of the nuclear accident pCi = 37 mBq After Aarkrog et al, 1977

33. Sample typeBiomass ( g m -2 ) Inventory in MBq 1970 1974 Transfer from release of 37 GBq ( in MBq y -1 ) Bivalve Molluscs: Soft parts Shell 100 88.8 70.3 222 185 55.5 148 Brittlestars30111 29.6 22 Shrimp2037 7.47.4 Worms1018.5 - Sediments-1.11 TBq - *Estimates of 239+240 Pu inventories and transfer-coefficients in sediments from Thule, Greenland contaminated in 1968 * Aarkrog et al, 1977

34. Summary of Some Needs for Future Marine Radioecological Studies At the base of the food chain, far fewer radionuclide data exist for phytoplankton communities than for zooplankton, and data are virtually non-existent for the picoplankton Radioecological data for zooplankton are derived mainly from studies on micro-crustaceans (i.e. copepods and euphausiids) and may not be applicable to the many other plankton taxa which have very different physical structures, physiologies, and feeding strategies Lab and field studies have demonstrated the role of zooplankton grazing in accelerating the transport to depth of radionuclides in large particles. Time- series sediment trap studies coupled with real-time sampling of zooplankton and their excretion products are now needed to examine at higher resolution these radionuclide scavenging and transfer rates For adequate models to assess dose from anthropogenic radionuclides, we need a broader database for natural radionuclides, particularly 210Po and 40K, in a variety of marine organisms and their tissues

35. Summary of Future Needs (cont.) More information for top trophic level marine mammals is required to establish adequate dose models for these species as well as for human consumption by certain populations Most data at present are derived from temperate mid-latitudes; similar information on radionuclide concentration factors and transfer rates is needed for tropical and polar regions to test the applicability of temperate zone data to those regions In future seas, increased temperatures and acidification may alter parameters like radionuclide speciation and resultant bioavailabilty, food chain structure, species composition, etc. Some effort to understand the behaviour and food- chain transfer of key radionuclides under such scenarios would be useful in making future predictions

36. Arigatou