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Radioactivity in the Marine Environment (1971)

Chapter: ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS

« Previous: MARINE SEDIMENTS AND RADIOACTIVITY
Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Page 170
Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Page 196
Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Suggested Citation:"ACCUMULATION AND REDISTRIBUTION OF RADIONUCLIDES BY MARINE ORGANISMS." National Research Council. 1971. Radioactivity in the Marine Environment. Washington, DC: The National Academies Press. doi: 10.17226/18745.
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Accumulation and Redistribution of Radionuclides by Marine Organisms 167 100,000 p- FIGURE 2 Relation of concentration factor of several elements in algae, phytoplankton, and zooplankton to their absorption from seawater by Chelex-100. III X o^* .*?** *• X 10,000' r * cf. / ' £1000 - X s ! /' «\ 1 I X * S *- X / _ Q. X / + X / " « /• x S 100 o IO'1^ * / I c - G6 c,< / ~ 1 / - » • - / - I rofc - S 10 _ i X ~ g : s / : 0 u ' ^, • - 2 ^ x/X - • * 1.0. . • / : I x x - + x ~ X O.I 1 -L 1 1 1 1 1 1 0 10 30 30 40 50 60 70 80 90 % absorbed from sea wafer by Chdex- 100 I00 factors are taken from a large number of references, and comparisons of factors between individual elements cannot be made in most cases; however, general patterns of uptake may be selected. Here, as described before, the alkali metals, sodium through cesium, and the alkaline earths, magnesium through radium, show a general increase in uptake with in- creased ionic radius. Beryllium, however, is concentrated more strongly than magnesium and calcium, although its ionic radius is much smaller. Beryllium has several proper- ties relating it to zinc and/or cadmium, including a ten- dency for covalent bonding, formation of complexes, and formation of amphoteric hydroxides. Beryllium thus might be expected to resemble, in part at least, the IIB elements in enhanced uptake by marine organisms. In general, the elements that are concentrated signifi- cantly in marine organisms (Table 1) may be grouped into at least one of five categories. These are (a) structural ele- ments: carbon, nitrogen, phosphorus (silicon, calcium, and strontium, in some cases); (b) catalyst elements: iron, cop- per, zinc, manganese, and cobalt (nickel, chromium, cad- mium, and silver may follow these elements); (c) elements easily hydrolyzed at seawater pH: aluminum, gallium, scan- dium, yttrium, cerium, plutonium, titanium, and zirconium; (d) heavy halogens: bromine and iodine; and (e) heavy diva- lent ions: barium, radium, and lead. Marine plants and animals concentrate the different iso- topes of a given element to the same degree, provided the isotopes are in the same chemical and physical form.* The degree to which radionuclides are incorporated into food webs also depends upon the availability of the correspond- ing stable element and metabolically similar elements and the physiological and behavioral characteristics of the orga- nisms in food webs and chains. Because several radionuclides are accumulated by marine organisms to concentrations several thousand times the amounts in the water, several investigators have suggested that biological transport may be a factor in altering their distribution in the sea. Investigations of the presence of radionuclides in the marine environment have been concerned mainly with the release of contaminants produced by nuclear technology, including testing of nuclear weapons, as well as reactor cool- ing and fuel processing. Radionuclides that are accumulated *Except for lighter elements, including H, C, O, and S (Vogel, 1969; Degens, 1967; Miinnich and Vogel, 1959; Ault, 1959a and b; Silverman and Epstein, 1958;Craig, 1954).

168 Radioactivity in the Marine Environment TABLE 1 Average Concentration Factors for Benthic Algae, Plankton, and Mollusc, Crustacean, and Fish Muscle" Chemical Group Benthic algae Phytoplankton Zooplankton Mollusc Muscle or Soft Parts Crustacean Muscle Fish Muscle IA Li - - - 0.28 1.2 0.47 Na — — — 0.2 0.3 0.13 K - - - 8 13 13 Rb - - - 16 13 17 Cs - - - 8 23 15 Ir - - - - - - IB Cu 100 30,000 6,000 5,000 - 1,000 Ag - 23,000 9.000 7,100 7 - An 470 - — 400 400 60 IIA Be 110 1,000 15 Mg 2 2 4 1 - 0.2 Ca 2 2.5 5 0.4 120 1.5 Sr 96 — - 1 3 0.1 Ba - 17,000 900 — - 8 Ra 1,400 1 2,000 190 1,300 140 130 1111 "Zn 410 15,000 8,000 11,000 2,000 500 Cd 200 — - - - 1,000 Hg - - - - - - 1IIA B <! 1.6 - — 2 AI 15.000 100,000 100,000 9,000 12,000 10,000 Ga 1,300 8,000 7,000 2,000 2,000 - In - - - - - - II - - - - - - 1I1B Sc 2,000 2,000 1,000 - 300 750 Y 480 1,000 105 12 - 250 La - - - - — — Ce 670 90.0006 1,000 360 2 0.3 Pu 1,300 2,600 2,600 260 3 3 IVA C -4,000 3,600 2,800 4,700 3,600 5,400 Si 100 2,000 300 50 - 20 Ge 50 — — - — - Sn .- 6,000 450 - - - Pb 700 40,000 3,000 40 - - IVB Ti 4,100 25,000 1 7,000 - - - Zr 2,200 60,000 25,000 2 2 <1 Hi - - - - - - VA N - 36,000 24,000 47,500 44,000 65,000 P 10,000 34,000 1 3,000 6,000 24,000 33,000 As 2,000 - - 650 400 700 Bi - - - - - - VB V 600 600 700 1,700 330 110 Nb 1,000 1,000 — 7 3 100 /Ta - - - - - - VIA S 1 0.3 1 Se 1 - - - — - Te - — - - — - Po 1,000 — - - — -

Accumulation and Redistribution of Radionuclides by Marine Organisms 169 TABLE 1 (Continued) Chemical Group Mollusc Muscle or Soft Parts Crustacean Muscle Benthic algae Phytoplankton Zooplankton Fish Muscle VIB Cr 1,600 2,400 1,900 440 100 70 Mo 8 - 26 60 10 10 W 5 - - 20 2 3 VIIA F 1 - - - - - a 1 1 1 1 1 1 Br — — — - - - I 5,000 - 3,000 S0 30 12 At - - - - - - VIIIB Mn 2,300 4,000 1,500 12,000 1,900 80 To — — — - - - Re - - - - - - VIII Fe 4,800 45,000 25,000 9,600 2,400 1,600 ,/Co 800 1,500 700 600 500 10 Ni 1,000 5,000 3,000 - - - Ru 390 200,000* 34,000* 3 100 0.05 Rh - — - - - — Pd - - - - - - Os - - - - - - Ir - - - - - - Pt - - - - - - "Data derived from Polikarpov (1966), Templeton (1965), Goldberg (1962), Vinogradova and Koval'skiy (1962), Fukai and Meinke (1962), Nit.hu11s ft al., (1959), and from unpublished work of Lowman. *Slowey etal. (1965). in easily detected amounts by marine organisms include the fission products 95Zr, "Mo, 103Ru, 106Ru, 1311,140Ba, 141Ce, 144Ce, and the neutron-induced radionuclides 32P, "Mn, 55Fe, 59Fe, 51Cr, "Co, 60Co, 65Zn, 110Ag, 181W, 185W, and 187W, and natural 40K. All of these radionuclides, except for 40K, represent stable elements that occur in sea- water at much less than one part per million. If marine organisms are capable of altering the distribution patterns of the radionuclides listed above from those expected to occur from physical and chemical factors in the sea, then they should also be capable of influencing the distribution of the corresponding stable elements. The present discussion will concern both stable and radioactive isotopes. Accumulation and Biological Transport In seawater the major or conservative stable elements are transported by currents as solutes, soluble chelates, or dis- persed colloids and may undergo limited movement from one water mass to another by eddy diffusion. Elements asso- ciated with biological material also are distributed by these processes but, in addition, are transported by vertical and horizontal migrations of animals, are anchored in place on the bottom through incorporation by benthic organisms, or are carried to the bottom from the surface by the effect of gravity on dead organisms, fecal pellets, moulted exoskele- tons, and other organic detritus. Any influence of marine organisms (or of physical or chemical processes) that changes the distribution pattern of an element from that of the conservative elements depends upon the conversion of the element from soluble or colloi- dal to particulate form. For marine organisms to change the distribution of a stable element (or radionuclide), they must alter a significant fraction of the total element present in the water in a period of time equal to or less than the time required for transport by water. This is most likely to occur if the radionuclide is introduced into an area of intense bio- logical activity in which there is a shortage of trace elements resulting from a high rate of utilization. The rate at which nutrients may be incorporated into phytoplankton is directly related to the biomass. However, the incorporation of nutrients is also limited by the amount of the organic material produced. Only those nutrients present in the euphotic zone at any given time may be in- corporated into the biomass. As the phytoplankton popula- tion increases, so does the absorption of light in the water.

170 Radioactivity in the Marine Environment Photosynthesis, thus, becomes more and more restricted to a thin layer near the surface in which nutrients are rapidly depleted. If vertical mixing occurs, bringing nutrients into the euphotic layer, the same mixing may carry phytoplank- ton to deeper waters where lower levels of illumination will reduce photosynthesis and eventually cause their death. In contrast to photosynthesis, which is restricted to a narrow layer at the surface, catabolism, excretion, death, and decomposition occur at all depths, including the eupho- tic zone. Over most of the oceanic area, there is a shallow upper zone of incorporation of elements, a downward movement of dead organisms and particulate excretion products, and a broader zone of regeneration; a net down- ward movement of nutrients occurs with time. The vertical distribution of the elements will depend upon the total amount of each element accumulated in the biomass, the sinking rate, and the rate at which the individual elements are regenerated into solution. Those elements regenerated more rapidly tend to remain in the upper layers, while those with slower regeneration rates become distributed into the deeper waters. Distribution of the Structural Elements Nitrogen, Phosphorus, Carbon, and Silicon Four structural elements-nitrogen, phosphorus, carbon, and silicon-are present in phytoplankton at levels from 1,000 to 40,000 times the amounts found in seawater. In some diatoms, the concentration factor for silica may be as high as 55,000. These concentration factors are of the same order of magnitude as those observed for the uptake of several radionuclides by these and other plankton. Thus, an examination of the distribution patterns of nitrogen, phos- phorus, carbon, and silicon in the waters of areas of high biological productivity may provide an insight into possible effects of biological activity upon radionuclide transport and distribution, provided turnover rates for the nutrient elements and the radiocontaminants are comparable. The elements carbon, hydrogen, nitrogen, and phosphorus are involved in the marine food webs as essential compo- nents of protoplasm and-particularly carbon and phos- phorus-as constituents of skeletal parts and shells. In plankton organisms these elements are found in atom ratios that approximate H:C:N:P= 268:106:16:1 (Sverdrup et al., 1942), which provided the basis for the C: N: P ratios and the hypothetical planktonic composition (CH.iO)lQO (NH3)16 H3PO4 suggested by Redfield et al., 1963. The C: N: P ratios exclude carbon in calcareous structures and phosphorus of skeletal structures of higher forms. The ra- tios of shell and skeletal carbon and phosphorus are highly variable, but reasonable limits of variability in the structures may be established. The amount of carbon, hydrogen, nitrogen, and phos- phorus that can be photsynthetically incorporated into plant material, and thus ultimately into animaJ material, is limited by the available supply and the stoichiometric com- position of the resulting biomass. Although it has been sug- gested that several elements may act as limiting parameters for the production of the total biomass, it is increasingly evident that the potential productivity of the sea is primar- ily a function of the availability of phosphorus or nitrogen or both. Potential fertility may be defined as the quantity of or- ganic matter that photosynthesis can produce in a volume of seawater if allowed to proceed until the limiting nutrient is exhausted (Redfield et al., 1963). Thus, the potential productivity is chemically limited and tends to represent upper limits of primary productivity. However, the limiting is not subject to a sharp cutoff, although phytoplankton normally assimilates nitrogen and phosphorus in the atom ratio of approximately 15:1 until very low concentrations of the nitrogen are present in the water. Even after the ni- trogen is almost completely depleted in the. water, the phy- toplankton cells apparently continue to incorporate phos- phorus, which is still present in relatively large amounts in solution (Ketchum et al., 1958). According to Ketchum et al. (1958), eddy diffusion may bring nitrogen and phos- phorus to the euphotic layer from the deeper layers in higher amounts than normally occurs in the euphotic layer; thus, the phytoplankton could use the element in short supply as rapidly as it became available. In this way, the phytoplankton would continue to form cells of normal composition and incorporate nitrogen, which apparently was present in extremely small amounts in the water. Even here, the rate at which nitrogen was supplied from the deeper water to the euphotic layer would exert a limiting effect. The maximum potential productivity of the open ocean is probably represented by the deep waters of the North Pacific where the phosphate content is about 3.5 X10~6 M. The photosynthetic utilization of all this phosphorus would take place as shown in Table 2. It is evident that, in the example chosen, the total realiza- tion of the potential productivity of this water would bind all of the nitrate, most of the phosphate, about 10 percent of the carbon, and a negligible fraction of the hydrogen into the bodies of the plants. Following the same reasoning used by Redfield et al. (1963), this would result in the fixation of 371 mg-atoms of carbon per m3* or 4.452 g of carbon per m3. If the carbon constitutes 50 percent of the dry weight of the plankton and the dry/wet ratio is 0.2, the wet weight of the plankton would be 44.5 g/m3. This is approxi- mately the biomass that has been observed in redtide blooms (41 cc/m3, Ketchum and Keen, 1948). If the plank- ton has a density the same as that of seawater, this amount of productivity would represent the following concentra- *3.5 mg-atom C/m3X 106 (atom ratio for carbon) =371 ing-atom C.

Accumulation and Redistribution of Radionuclides by Marine Organisms 171 TABLE 2 Amount of Nutrient Elements in "Richest" Seawater and the Rates of Availability and Utilization by Phytoplankton (1) (2) mg-Atoms/m3 in Richest Seawater (3) Relative Availability in Richest Seawater (4) Atom Ratio Utilized in Phytoplankton (5) Relative Availability (3)/(4) Element P (P04) 3.5 1 1 1 N (N03-) 52.5 IS 16 0.94 C(HC03-) 3,559.5 1,017 111 9.6 H (H20) 108,000,000 30,850,000 260 1.2X10s tion factors: phosphorus: 2.2X104; nitrogen: 2.4X104; carbon: 2.3 X103; hydrogen: 0.195. Nowhere has the estimated annual production of plank- ton populations been observed to exceed the potential pro- ductivity of the richest oceanic water cited above, assuming a photic depth of 50 m. If the mg-atom ratios for the four elements in "average" seawater were used (P= 2.3; N = 34.5; C = 2,340; H= 1.08 X108) instead of those for "richest" sea- water, 244 mg-atoms or 2.93 g of carbon per m3 would be fixed. This would amount to 29.3 g of wet plankton per m3. The concentration factors for the four elements under these conditions would be, for phosphorus, 3.4 X 104; for nitrogen, 3.6 X104; for carbon, 3.6 X103; and for hydrogen, 0.195. In each case, the concentration factors for phosphorus and nitrogen are approximately 3 X104; carbon, 3 X103; and hydrogen, 0.2. These concentration factors are prob- ably representative for all of the more productive areas of the world. The potential productivity in the vicinity of Woods Hole, Massachusetts, might be assumed to be related to a concentration of phosphate of 2 X10~6 M (62 ^g P/ liter). This could yield 2.54 g C/m3 or, in a photic zone 50 m deep, 127 g C/m2. A weighted mean average for the region is 120 g C/m2/year (Ryther, 1963). This agreement is probably fortuitous, but it might be interpreted as mean- ing that, at the average rate of production it would take a year for all of the phosphate and nitrogen in the photic zone to be incorporated into the bodies of plants and animals and that replacement water, if any, had the same produc- tivity potential when introduced into the photic zone. The turnover rates for nitrogen and phosphorus may equal or exceed, in a short-time interval, the annual average, and the fractions of both elements that are not passed to higher trophic levels or to the bottom through the sinking of fecal pellets, moults, and dead organisms are probably recycled between the primary producers and the water sev- eral times during an annual cycle. Even the degree of association suggested by the annual average for the accumulation of other elements is sufficient that local populations with movements independent of the motion of the water would be expected to contain and transport significant amounts of total phosphorus and ni- trogen accumulated in the euphotic layer. If the marine organisms do indeed transport nitrogen and phosphorus in patterns different from those resulting from physical mech- anisms, they might also be expected to exert a similar influ- ence upon the distribution patterns of other elements, and their radionuclides, that are accumulated to the same level. The nutrient elements do exhibit vertical distribution patterns different from those of the conservative elements (Figure 3). Phosphate, nitrate and silica are found in the in- termediate and deep water in greater amounts than in the euphotic layer. These three elements may be removed from the surface layers by the settling of phytoplankton; by in- corporation of the phytoplankton into the zooplankton, which undergo diurnal migration; or by excretion or loss as fecal pellets, moults, dead zooplankton, and organic debris, all of which will sink. Most of the phosphorus in the animals undergoes rapid turnover. Varying amounts of it are incorporated into fecal pellets, other excretory products, dead organisms, and into the skeletal structure of fishes, which are deposited upon the bottom after the death of the animal. Skeletal apatite slowly dissolves in the deeper parts of the ocean, and a large part of the phosphorus is eventually returned to solution in these areas. Upon the death of phy toplankton and zooplankton, phosphorus appears to be regenerated back into the water slightly more rapidly than nitrogen, and nitrogen more rap- idly than carbon, since the C : N : P ratios increase with depth (Richards era/., 1965; Holm-Hansen et al., 1966; Vaccaro, 1963). However, the relative regeneration rates of carbon and nitrogen may vary according to local conditions, since Menzel and Ryther (1964) observed low ratios of car- bon to nitrogen below the euphotic zone to depths of 4,000 m and reported that similar conclusions could be derived from the data of Parsons and Strickland (1962). In any event, the turnover rate of phosphorus is sufficiently rapid that large variations of phosphorus concentration with time of day have been noted in Chesapeake Bay (Newcombe

172 Radioactivity in the Marine Environment mg of P04 - P/m 10 20 30 40 mg at N0, - N/m 10 2O 30 40 IOOO *n K UJ U z 2000 £ U a 3000 a 3000 4000 ATLANTlC/ PAC1FIC / IND1AN -1 u 1 1000 2000 - 3000 FIGURES The vertical distribution of phosphate, nitrate and silica in the Atlantic, Pacific, and Indian oceans. (Reprinted with permission from Sverdrup et al., 1942.) and Lang, 1939), with the phosphate in the surface waters decreasing slowly after sunrise from 13 jug P/liter to a mini- mum value of 3 Mg P/liter at 3:00 p.m. After sunset, the phosphorus increased rapidly to maximum values about 2 hours after midnight. Newcombe and Brust (1940) reported similar observations. Phosphorus is also turned over rapidly in dead or dying phytoplankton. Hoffman (1956) reported that, upon the death of diatoms, autolysis rapidly released up to 25 percent of the total phosphorus as inorganic phos- phate. Raymont (1963) observed that immediately after death of phytoplankton about one third of the total phos- phate was released as dissolved organics and that within 2 days, 70 percent of the remaining phosphorus was reminer- alized. Menzel and Ryther (1964) stated that, in comparison to carbon and nitrogen, phosphorus was regenerated very rapidly, since no phosphorus was found associated with or- ganic particulates at depths below 200 m in the western North Atlantic. In some cases, the regeneration of phosphorus in zoo- plankton may be even more rapid than in phytoplankton. Pomeroy et al. (1963) reported that zooplankton were ca- pable of excreting 100 percent of the contained phosphorus daily, a large part of which was apparently tied up in soluble organic compounds and was not excreted as phosphate. The regeneration of silica from diatom skeletons might be expected to differ from phosphorus in that the regenera- tion of phosphorus and nitrogen involves the removal of both elements as constituents of organic matter. In addition, zooplankton incorporate phosphorus and nitrogen, but not silica. The silica tests are ejected and would sink to dissolve at greater depth while the two other elements would be re- tained in the upper layers (Redfield et al., 1963). In summary, the vertical distribution of phosphorus, nitrogen, and silica in the sea is affected by biological trans- port, and the concentrations of the three elements are not related to salinity or the distribution of the conservative elements. The vertical distributions of the three elements differ in the Atlantic, Pacific, and Indian oceans (Figure 3) but follow a generally similar pattern. Phosphorus, nitrogen, and silica are usually present in the surface waters in low amounts or are depleted and rise gradually in value to a maximum for phosphorus between 300 and 1,000 m, but for nitrogen and silica the maximum is at 1,000 m or deeper. Carbon is concentrated by phytoplankton at factors about an order of magnitude lower than phosphorus or ni- trogen, and only about 10 percent of the available carbon dioxide is utilized under conditions of maximum uptake. The total amounts of carbon dioxide increase with depth because of its incorporation into plants in the euphotic layer and the production of carbon dioxide when dead ma- terial is oxidized at deeper levels. Low oxygen concentra- tions and pH values in areas with relatively large amounts of carbon dioxide tend to characterize water masses that are poorly ventilated and that receive large amounts of decay- ing organic matter (Skirrow, 1965). Carbon dioxide con- tent of seawater often increases measurably with depth in the first few hundred meters. Keeling et al. (1965) reported observations from the equatorial Pacific in which the carbon dioxide increased from 310 ppm in the top 100 m to a value of 620 ppm at 450 m. The oxidation of carbon compounds appears to proceed more slowly in those containing nitrogen (i.e., the proteins). Thus, Menzel and Ryther (1964) observed that the C:N ra- tios in nonliving detritus collected in the euphotic zone were the same as those in living phytoplankton (C: N 11.5:1 in January and 5.3:1 in April). In the deeper wa- ters, to depths of 4,000 m, the C: N ratio decreased to 2.5:1. The average C: N ratio for protein is about 2.9:1 (Sverdrup et al., 1942). Menzel (1967) reported, however, that the surface standing crop at any given site had no influ- ence on the amount of organic particles directly below- that the distribution of organic particles in all areas of the sea was homogeneous in the deeper waters and that no con- sistent decrease in dissolved carbon occurred with depth. Redfield (1942) considered that, in the North Atlantic, the high nutrient levels at depth were derived from material

Accumulation and Redistribution of Radionuclides by Marine Organisms 173 sinking at the Antartic Convergence. Sheldon et al. (1967) also found that between depths of 200 and 4,000 m the amount of particulate carbon was constant in different areas of the sea. Hobson (1967), however, observed seasonal and vertical variations in particle concentrations in the north- east Pacific Ocean. He tentatively attributed these variations to differences in the production of particles in the euphotic zone and their subsequent sinking and horizontal transport by currents. Uptake of Nonstructural Elements and Their Radionuclides by Phytoplankton Twenty-six elements have been reported to be concen- trated in marine organisms by factors approximately equal to or greater than that for carbon. In addition, plutonium, which occurs naturally in only insignificant traces but is produced by man, has been observed to be accumulated by mixed plankton to levels 2,600 times those in the surround- ing water (Pillai et al., 1964). Those elements that are concentrated at least 1,000 times in marine phytoplankton are shown in Table 3. Also shown are the radioisotopes most likely to be formed by fission and by activation by neutrons, protons, deuterons, and alpha particles. Except for a few radionuclides, only those resulting from fission and neutron activation would be produced in relatively large amounts. Of the 25 radio- nuclides listed, 28A1, 76As, MCu, 131I, and 47Sc have short physical half-lives and would undergo physical decay before biological transport could significantly alter their distribu- tion in the oceans. Of the remaining nuclides, two,i 15mCd and 63Ni, would not be produced in large amounts by known sources (Beasley and Held, 1969). Thus, 7 of the 25 radionuclides listed in Table 3 would not have radioiso- topes subject to significant biological accumulation and may be eliminated from further consideration. The remain- ing 18 radionuclides include several of known biological importance. These include 32P, 54Mn, "Fe, 59Fe, "Co, 58Co, 60Co, and 65Zn. The radionuclides of elements that do not have known biological functions include 46Sc, 95Zr, 95Nb, nomAg, 144Ce 2ioPb and 239Pu Of special interest is the observation that, of the above- TABLE 3 Elements Accumulated by Phytoplankton to Levels at Least 1,000 Times Those in Seawater and Principal Radionuclides of Interest in Considerations of Biological Transport Element Radionuclide Half-life Principle Reaction for Production Reported Concentration in Phytoplankton Al 28A1 2.31 mina 27Al(n,7) 1X 10s As 76As 26.4 hr" 75As(n,7) - Be 7Be 53.6 day 6Li(d,n)6 1X103 C 14C 5,730 yr 14N(n,p) 4X103 Cd 115mCd 43 day ' 114Cd(n,7)6 - Ce 144Ce 275 day Fission 9X104 Or 51Cr 17.8 day 50Cr (n.7) 2X103 Co "Co 270 day 56Fe(d,n) 1X103 56Fe(p,7) Co 58Co 71. 3 day 55Mn(a,n) 1X103 - Co 60Co 5.26 yr 59Co(n,7) 1X103 Cu 64Cu 12.8hr" 63Cu(n,7) 3X104 I 131j 8.05 day" Fission - Fe "Fe 2.6 yr 54Fe(n,7) 4X104 Fe 59Fe 45.6 day 58Fe(n,T) 4X104 Pb 210pb 20.4 yr Daughter 226Rac 4X104 Mn 54Mn 303 day 56Fe(d,a);54Fe(n,p) 4X103 Ni 63Ni 92 yr 62Ni(n,7>6 5X103 Nb 95Nb 35 day Fission 1X103 P 32p 14.3 day 31P(n,7) 3X104 Pu 239pu 24.4 yr 238U(n,7) 2.6 X103 Sc 46Sc 83.9 day 45Sc(n,7) 2X103 Sc 47Sc 3.43 day" Daughter 47Ca - 4°Ca (n, y) 2X103 Ag 110mAg 255 day 109Ag(n,7) 2X104 Zn 65Zn 245 day 64Zn(n,7) 2X104 Zr 95Zr 65.5 day Fission 6X104 " Radionuclide has too short a half-life for effective biological transport. "N.* known source of large-scale production. Small-scale production of °3Ni reported by Beasely and Held, 1969. Pb reported to be formed in explosives used for peaceful uses of nuclear explosives.

174 Radioactivity in the Marlne Environment listed radionuclides, all except 210Pb have been reported to be concentrated by marine organisms from radioactive con- tamination introduced into the sea from nuclear weapons test sites and from outflows from production reactors and reactor fuel reprocessing plants. Lead-210 has not been produced in sufficient amounts by nuclear explosives to have been studied in detail. Naturally occurring 210Pb has been reported in marine organisms (Beasley et al., 1969). Biological Transport by Zooplankton Phytoplankton and zooplankton are the marine organisms most likely to influence the distribution patterns of radio- nuclides introduced into the sea. These organisms constitute the largest biomass, have the greatest total exposed biologi- cal surface areas, exhibit the highest concentration factors and turnover rates for many trace elements, and, in the case of zooplankton, migrate vertically. The magnitude and ex- tent of diurnal vertical migration of zooplankton living in the upper layers, however, is often overestimated, and the plankton populations are sometimes considered to corre- spond to a large biological "blotter," which daily moves up and down to great depths, scavenging and redistributing radionuclides and trace elements in its path. Plankton, to significantly alter the distribution of radio- nuclides from that caused by physical and chemical pro- cesses, must effectively transport the material at rates com- parable with movement due to currents, turbulent diffusion, density gradients, and chemical precipitation or must alter the availability of the radionuclides for physical transport processes. Biological transport may be accomplished by direct uptake and loss of the radionuclide accompanied by horizontal or vertical movement, by the excretion of fecal pellets, and by the sinking of moulted exoskeletons or dead or moribund plants and animals. Direct transport of radionuclides by vertical migration of zooplankton is dependent upon the ability of the organisms to travel relatively great distances in comparison with their size. In many areas of the world, the upper mixed layer is 80 to 100 m deep, and effective transport by the plankton may thus occur only if they migrate vertically beyond this depth. Diurnal Migration of Deep-Water Plankton and Biological Transport Up from Depths Vertical migrations of zooplankton through great distances have been reported for some species, and the importance of these migrations has sometimes been given undue empha- sis, since these species constitute only a small fraction of the total zooplankton populations. ZooplanJcron exist at great depths in the sea; however, their diurnal vertical mi- grations are usually limited to a few hundred meters, and the ratio of their volume to that of the water is usually of the order of 10~8. Amphipods, copepods, and ostracods have been collected from depths of 6,000 to 7,000 m by Russian investigators (Wolff, 1960), and concentrations of zooplank- ton have been observed at 1,500 to 2,000 m in the Atlantic (Leavitt, 1938). A significant fraction of these deep-living zooplankton undergo migrations although the depths at which they live preclude regular excursions into the upper mixed layer. Waterman et al. (1939) showed that amphipods, decapods, euphausids, and mysids migrated from 1,000 m upward to 200 to 600 m, and Bainbridge (1961) reported that the upper limit of migration for Thysanopoda acuti- frons and Acanthephyra purpurea was about 200 m below the surface. The zooplankton from the deeper waters would, therefore, exert much less effect upon vertical trans- port of surface-introduced radionuclides than the animals in the upper layers, because those in deeper waters consti- tute a relatively small portion of the total population, and most of them do not pass into the upper mixed layer. Ketchum and Bowen (1958) calculated the relative effec- tiveness of vertical transport of elements upward from the deeper waters by biological and physical processes using the mean residence time of 300 years (Craig, 1957) in the deep water (assuming an average depth of 3,800 m and a 100-m upper mixed layer). They reported that a concentra- tion factor of 340 in zooplankton would be required for upward biological transport to equal that provided by phys- ical transport. The numerical values used in these calcula- tions, however, represented conditions that would result in near-maximum biological transport. They probably are not typical of the usual conditions. The ratio of zooplankton volume to water was assumed to be 10~6 and corresponds to the biomass of zooplankton found in areas of upwelling, which are sites with high rates of biological productivity. In many areas of the sea, smaller amounts of zooplankton are found. In addition, plankton in deeper waters are usu- ally present in smaller quantities than in the surface layers. Bogorov (1946) found that 95 percent of the zooplankton in the Artic seas lived in the upper 200 m and only 5 per- cent of the total were below this depth. Even if the zoo- plankton in the deeper waters constituted four times this amount, the results cited above would be high by a factor of four. The calculations were based upon the premise that the animals reached equilibrium with the radionuclides during the time spent in each water layer. This would require rapid turnover rates. In a study of zooplankton contaminated with radionuclides, Kuenzler (1965) found hourly turnover rates of 1 to 6 percent of the body pool for 131I, 54Mn, 58Co, 60Co, 55Fe, and 65Zn. In the copepods, which constituted 62 percent of the total zooplankton, the rates were 2.4 per. cent/hr for 131I,4.5 percent/hr for 58Co and 60Co, and

Accumulation and Redistribution of Radionuclides by Marine Organisms 175 1.2 percent/hr for 65Zn. Turnover rates of this magnitude could result in organisms approaching equilibrium at least for cobalt, if the observed rates of turnover were maintained continuously. These values, however, as well as most others that have been reported, were measured at surface tempera- tures. At these temperatures the turnover rates are 1.5 to 3.5 times those that occur in the deeper, cooler waters con- sidered in the calculations. If those factors are taken into account, as well as the effect of vertical plankton distribu- tions, concentration factors of about 104 would be required for biological transport upward to equal physical transport. The average ratios of zooplankton volume to water in different marine areas have been tabulated by Ketchum (1957). Shown in Table 4 are the locations, the zooplankton biomass, and the concentration factors required for a rate of biological transport upward that would equal physical trans- port. The concentration factors are corrected for tempera- ture and vertical distribution of plankton as described previously. Mean concentration factors (CF) in zooplankton rarely exceed 104, as shown in Table 1. Elements that are concen- trated to the highest level by zooplankton include aluminum (CF 100.000), zirconium (CF 25,000), nitrogen (CF 24,000), titanium (CF 17,000), phosphorus (CF 13,000), and iron (CF 25,000). Only zirconium, phosphorus, and iron have radionuclides that are normally produced in nuclear tech- nology. For these radionuclides, biological transport from the bottom waters upward would be significantly lower than physical transport in all open ocean areas cited in Table 4 because of the relatively low concentration factors that exist for these elements. In the nearshore areas, includ- ing the Gulf of Maine, coastal waters, and the North African Upwelling, physical transport from deeper waters to the surface is at least one order of magnitude greater than the Atlantic average, and here also, physical transport would be more effective than biological transport in moving radio- active contaminants from the deeper waters to the surface. Diurnal Migration of Zooplankton from the Upper Mixed Layer and Biological Transport Down from the Surface Although zooplankton in the deeper waters may not con- tribute significantly to the transport of radioactivity from the bottom to the surface, surface-living species may trans- port relatively large amounts of radionuclides downward. Several authors have reported that the greatest amounts of zooplankton are found in the top 800 m of the sea and that most of the animals appear to live in the top 400 m. Johnson (1957) reported that during the daytime a major part of the diurnally migrating plankton was concentrated in one or more horizontal layers down to 400 m. Bogorov (1946), as mentioned before, observed that 83 percent of the zooplankton lived in the top 10m of Arctic waters, while 12 percent lived between 10 and 200 m and 5 percent lived between 200 and 750 m. This general pattern of verti- cal distribution does not appear to be limited to the polar regions. Fraser (1936) showed that the larval stages of Euphausia superba lived at about 200 m and migrated up- ward diurnally. The young stages of the same species re- mained near the surface and did not migrate vertically at all. Calanus finmarchicus, the major copepod in the North At- lantic, occurs in surface waters at night and migrates down- ward to a midday depth of about 70 m (Nicholls, 1933). According to Farran (1947, 1949) marine ostracods appear at two levels, one at 100 to 300 m and the other at 250 to 400 m. Michael (1911) showed that Sagitta bipunctata mi- grated between the surface and a depth of 50 m off Cali- fornia, and Hardy and Gunther (1936) reported that the amphipod Parathemisto migrated from the surface to a depth of 80 to 100m. According to Bainbridge (1961), the available data showed that most marine copepods migrated vertically 50 to 150m but that vertical movements could not be demonstrated forAnomalocerapatersoni,Rhincala- nus gigas, Calanoides acutus, Microcalanus pygaeus, Oithona TABLE 4 Biomass of Zooplankton in Different Marine Waters" and the Concentration Factors Required for Zooplankton to Transport Radionuclides Upward at a Rate Equal to the Physical Transport Location and Character Volumes (cc) of Zooplankton/m3 Concentration Factors Required for Equal Biological and Physical Transport Upward Sargasso Sea Eastern North Pacific 0.006-0.09 0.042 75,000-1,000,000 55,000 Eastern Tropical Pacific Peru Current 0.055 0.124 40,000 55,000 Gulf of Maine Coastal waters 0.08-1.0 0.08-0.8 6,800-85,000 8,500-85 ,0006 North African Upwelling 1.0 6,800 "Data from Ketchum (1957). *Not directly applicable because the rates of vertical transport from physical processes in these areas greatly exceed the rates used for the open sea. The concentration factors shown are correspondingly low.

176 Radioactivity in the Marine Envjronment frigida, and Centropages typicus. In some cases, zooplankton will not move into the upper mixed layer from deeper wa- ters if a thermocline is present (Clarke, 1934). The observations cited above, and others, suggest that the majority of zooplankton inhabit a relatively thin upper layer of the sea. This should be expected since the upper few meters constitute the site of major food production. Except for the settling of moribund and dead phytoplank- ton, the herbivorous zooplankton must feed in the upper layers of the sea, since net production occurs only above the level at which the oxygen produced by photosynthesis equals that consumed by metabolic processes in the auto- trophs. In the temperate regions, this depth is usually 5 to 50 m (Marshall and Orr, 1928; Clarke, 1946) although it may extend to 150 m in tropical waters (Riley et al., 1949; Wimpenny, 1966). Soluble-colloidal radionuclides introduced at the surface of the sea distribute through the mixed layer by physical processes but do not diffuse rapidly down through the pycnocline. Those plankton that normally live below the mixed layer must move into the upper mixed layer to be able to accumulate radionuclides directly from the water or to feed upon contaminated phytoplankton. If they derive their food from sinking organisms, detritus, or particulate excretory products or if they prey upon zooplankton that have moved down from the mixed layer, then the food must have been in the upper mixed layer in order for these deep-living zooplankters to become significantly contami- nated. Large sources of detritus would be required in the upper zones of the sea to support significant populations of detritus-feeding zooplankton. The food for these animals, derived from plants and animals living in contaminated sur- face waters, would contain varying amounts of radionu- clides. Incorporation of radionuclides would occur through metabolic uptake by the food organisms or through accumu- lation directly onto the nonliving debris by adsorptive pro- cesses. Detritus often accounts for from 40 percent to more than 90 percent of the suspended organic particulates in the upper mixed layer where phytoplankton are most abun- dant (Krey, 1961), and this nonliving material may provide significant amounts of food and radionuclides for omnivores if its origin is in the upper mixed layer. Because the primary source of food is in the surface layers of the sea and usually decreases in amount with depth, it is not surprising that the herbivorous and omnivorous zooplankton live mainly in the upper waters. Carnivorous zooplankton must feed where their prey are available, and although they may have a greater vertical range than the omnivores and herbivores, they, too, often tend to become concentrated in the upper layers. Zooplankton living in the upper mixed layer metabolize radionuclides whether or not they migrate into deeper wa- ters during the daylight hours. For those zoopiankton that do not undergo vertical migration in and out of the upper mixed layer, all of the biological transport of radionuclides into the deeper water would result from the influence of gravity upon fecal pellets, moulted exoskeletons, and dead animals. At equilibrium, the only fraction of the ingested radionuclides that would not be carried down by this mech- anism would be that incorporated by growth and the amounts excreted by the animals back into the water of the mixed layer in soluble or colloidal form plus the fraction of the radionuclides dissociated into solution or colloidal sus- pension from the fecal pellets and moults as they settled. If migrating and nonmigrating individuals feed at equal rates in the surface waters, individuals that migrate downward diurnally from the mixed layer would not incorporate as much radionuclide into their body structure or into fecal pellets per 24 hours as would those animals not migrating, because of the shorter time spent in the contaminated zone. In the migrating forms, only a fraction of the total ingested radionuclide would be transported by vertical migration. The remainder would be transported by fecal pellets and moults. Since filtration rates of zooplankton generally de- crease with decreased temperature (Raymont, 1963), the zooplankton remaining in the warmer surface waters would ingest more food per day than those migrating to the colder deeper waters where their metabolic rates would also de- crease. One of the most definitive investigations of the role of zooplankton in the incorporation, turnover, and transport of a radionuclide by vertical migrations in and out of a con- taminated marine environment was carried out in the Pacific Ocean by Kuenzler in 1962 (Kuenzler, 1965,1969). In the area sampled by Kuenzler, the copepods consti- tuted 62 percent of the total plankton to a depth of 500 m, and 34 percent to 40 percent of this group stayed in the upper mixed layer at all times of the day. This distribution is in general agreement with those observed by Nicholls (1933) and other investigators. The total volume of plank- ton, down to a depth of 500 m, was only 6.8 g/m2. An average 4 g/m2, or 58 percent of the total zooplankton, spent at least part of each day in the upper mixed zone, at depths less than 100 m. About 41 percent of the plankton in the surface layers underwent diurnal migration down into the thermocline. Thus, only about 24 percent of the total zooplankton population, living to a depth of 500 m, mi- grated in and out of the upper mixed layer into which the radioactivity was introduced. This observation is in contrast with the assumption often made that a major fraction of the zooplankton participate in vertical biological transport of radionuclides out of the upper mixed layer. If the amounts of migrating and nonmigrating zooplank- ton in the upper mixed layer are known, one may estimate the relative efficiency of vertical transport by the different

Accumulation and Redistribution of Radionuclides by Marine Organisms 177 biological mechanisms, including diurnal vertical migration and the sinking of fecal pellets and dead or moribund ani- mals. The relative effect of these different transport mech- anisms is modified by several biological processes, including (a) feeding rates, (b) food utilization, and (c) the relative utilization of trace elements and radionuclides by zooplank- ton compared with that for nutrient elements. Effects of Feeding Rates and Utilization Efficiencies upon Vertical Transport Feeding rates in zooplankton are highly variable and subject to the influence of many physical and biological limits. An average value for daily ingestion of food equal to about 30 percent of their own body weight appears to be a good esti- mate for zooplankton. Riley (1947) observed thalAcartia required a daily amount of food equal to almost 30 percent of its own weight, and Smayda (1966) is of the opinion that the value may sometimes equal 100 percent. At the higher feeding rates, however, the rate of utilization of the ingested food is reduced, primarily as a result of rapid passage of the material through the gut, with limited digestion. The utilization of ingested food, like the feeding rate, is highly variable both within and between species of zoo- plankton. Part of this variability is due to differences in the fraction of ingested food excreted or voided as feces (Strickland, 1965). A low utilization efficiency would re- sult in enhanced transport of food material to deeper water layers by descending fecal pellets. A high utilization effi- ciency would favor transport downward by metabolic turn- over in zooplankton undergoing diurnal vertical migration. A utilization efficiency of 10 percent between trophic levels has sometimes been assumed; however, direct mea- surements of food conversion in several species of marine zooplankton suggest that efficiencies may be significantly greater than this. Reeve (1963) wrote of his investigation on growth efficiency in Artemia salina, "The work reported... indicates that the conversion of plant to animal tissue could, by special choice of conditions, be maintained at an effi- ciency of well over 50%." Conover (1964) fed Calanus hyperboreus three species of phy toplankton and reported "if the average caloric content of the algae ... are used to recompute the gross growth efficiencies... greater than 60% efficiency can be attained when food concentrations are relatively low." Monakov and Sorokin (1961) observed 40 percent effi- ciency in food utilization by the freshwater zooplankter Daphnia pulex, and efficiencies for marine zooplankton have been reported as follows: Organism Efficiency for Food Conversion (%) Reference Calanus 50-80 Marshall and Orr, finmarchicus 1955 Calanus 60-78 Marshall and Orr, finmarchicus 1956 Artemia 10-55 Gibor, 1957 Calanus 14 Gushing, 1955 Euphausia 10-70 Lasker, 1960 paciflca Calanus 74-91 Corner, 1961 helgolandicus Temora 50-98 Berner, 1962 longicornis Calanus 15-20 Conover, 1962 hyperboreus Artemia 9-20 Mason, 1963 Artemia up to 60 Reeve, 1963 Calanus 10-99 Mullin, 1963 In the genus Calanus, the conversion efficiencies varied from 10 to 99 percent with an average value of about 50 percent for the six experiments. The low conversion values reported for Artemia by Mason (1963) were postulated by Reeve (1963) to be partly due to the animals not being offered the optimum amounts of food necessary for maxi- mum growth; very small or very large amounts of available food reduce the utilization efficiencies. At a given low level of phy toplankton, the cell concentration passing through the gut of a zooplankter would be sufficient only to main- tain metabolic function with no excess left for building of new tissue. At high concentrations of phy toplankton, the pressure from incoming food would move the gut contents through at rates greater than those allowing efficient diges- tion and assimilation (Reeve, 1963). Although the average conversion efficiency in nature may be well below 50 percent, laboratory data do not con- firm this view. In the present considerations, a conversion of 50 percent of the ingested phy toplankton into second trophic level matter is assumed. This would tend to empha- size the role of direct biological transport by vertical migra- tion of zooplankters from a surface contaminated area in comparison with transport downward by fecal pellet pro- duction if the conversion efficiencies are indeed lower than 50 percent under field conditions. A conversion factor of 50 percent for organic material (based on carbon) does not necessarily indicate an equal conversion factor for all of the trace elements and radio- nuclides incorporated into, or associated with, food. In many cases, the conversion factors in the zooplankters for elements that have no known biological functions and for

178 Radioactivity in the Mar'fie Environment the catalyst elements are lower than those for carbon. This results in lower concentration factors for zooplankton com- pared with the amounts of the element or nuclide in the water. It also results in increased amounts of these elements in the excretory products of the zooplankton, relative to carbon and nitrogen compounds. Silica is an example of an element strongly accumulated by phytoplankton but not by zooplankton. Concentration factors in marine phytoplankton and zoo- plankton may be used to provide estimates of the efficiency of utilization of different elements by zooplankton. Conver- sion efficiencies may be obtained by relating the concentra- tion factors of the other elements to those for carbon in the two trophic levels. If the conversion factor for phytoplank- ton carbon is 50 percent in actively feeding zooplankton, then elements with the same ratios of concentration factors in the two trophic levels will also be utilized by the zoo- plankton at an efficiency of 50 percent, under equilibrium conditions. Thus CF cp X 0.5 X 100 X CF_, where Conv.efe(%) is the conversion factor in percent for the element by zooplankton, CF is the concentration fac- tor for carbon in phytoplankton, CFcZ is the concentration factor for carbon in zooplankton, CFelp is the concentra- tion factor for the element in phytoplankton, and CFel2 is the concentration factor for the element in zooplankton. The major weakness in this method of calculating con- version factors for a variety of elements is the uncertainty of the accuracy of the concentration factors for phyto- plankton and zooplankton. Relatively few analyses have been made on phytoplankton and zooplankton collected from one area. Vinogradova and Koval'skiy (1962) did analyses for 25 elements in 4 species of phytoplankton and 7 species of zooplankton collected in the Black Sea. The present calculations for relative concentration factors in the two trophic levels are based upon these and other m^asure- ments for individual elements. Concentration-factors may be calculated by two methods: (a) comparison of direct analyses of the stable element in the organism and in the water and (b) comparison of the amount of a radioactive tracer accumulated by an organism at equilibrium with the amount of the radionuclide in an equal weight of water. Both methods are subject to sampling and analytical errors. In addition, variations in species characteristics, environ- mental factors, biological condition of the experimental organisms, and changes in population densities, especially for phytoplankton in the exponential growth phase, may introduce further errors. Estimates for the utilization efficiencies for several ele- ments by zooplankton feeding on phytoplankton are shown in Table 5. The conversion factors are based upon an as- sumed 50 percent conversion efficiency for carbon. Conversion factors in zooplankton are low for barium (3 percent), radium (1 percent), yttrium (7 percent), cerium (3 percent), silicon (1 percent), tin (5 percent), and lead (5 percent). On the basis of these estimates, only small amounts of the seven elements would be incorporated into the biomass of the second trophic level, and almost all of the ingested elements would be excreted in fecal pellets and other excretory products. Fecal pellets appear to pro- vide the major transport mechanism for these trace elements and their radionuclides out of the mixed layer into the deeper waters. This agrees with the observations that those elements with low conversion factors, including barium, cerium, silicon, and 210Pb, have been shown to occur in larger amounts in deeper waters than in surface layers of the sea (Chow and Goldberg, 1960; Hogdahl et al., 1968; Rama etal., 1961; Goldberg and Koide, 1963). Zooplankton have intermediate efficiencies of utilization for the following elements: zinc (20 percent), scandium (30 percent), copper (13 percent), zirconium (30 percent), phos- phorus (25 percent), silver (25 percent), manganese (20 per- cent), chromium (28 percent), titanium (17 percent), and cobalt (30 percent). The zooplankton would excrete or void 70 to 90 percent of these elements. Of the elements with intermediate conversion factors, silicon and phosphorus show large increases in the water with depth in the open sea. Skeletal silicon tests of diatoms are known to pass intact through the gut tracts of zooplankton and to be voided in the feces; thus, this element would be subject to efficient transport to deeper waters with limited dissolution on the way down. Some phosphorus would be transported to deeper waters through the sinking of dead and moribund phytoplankton and zooplankton. In addition, part, at least, of the 75 percent excreted or voided phosphorus would be combined in the fecal pellets as insoluble phosphates of calcium, strontium, barium, radium, yttrium, cerium, and chromium and would be carried to deeper waters by gravity. On the basis of the estimates shown in Table 5, more than 40 percent of the ingested nitrogen, strontium, iron, aluminum, gallium, and zinc are converted into biomass by zooplankton. This is true for carbon and nitrogen; however, the high values for iron, aluminum, and gallium are prob- ably due largely to adsorption of hydrated hydroxides of these elements onto the surfaces of zooplankton, with an ensuing low rate of loss. The relatively high values (30 per- cent) for the apparent conversion of scandium and zirco- nium, elements with no known biological functions, are probably also due to this mechanism. Excreted fecal ma- terial, as well as the surfaces of zooplankton, would also be expected to provide adsorptive surfaces for these elements, with resulting transport downward.

Accumulation and Redistribution of Radionuclides by Marine Organisms 179 TABLE 5 Estimates of Efficiency of Retention for Zooplankton Feeding on Phytoplankton" Concentration Factor Conversion Factor, Phytoplankton to Zooplankton (%) Concentration, Deep Water/Surface Water Chemical Group Element Phytoplankton Zooplankton IB Ag 23,000 9,000 25 >1» Sr 21 28 85 1 IIA Ba 17,000 900 3 4 Ra 12,000 190 1 *•4 IIB Zn 26,000 8,000 20 1.8c IIIA Ai 100,000 100,000 60 - Ga 8,000 7,000 60 - IIIB Sc 2,000 1,000 30 - Y 1,000 105 7 - Ce 4,000 3 ~4 IVA Si 17,000 300 1 M00 Sn 6,000 450 5 — Pb 40,000 3,000 5 -2.5 IVB Ti 25,000 6,800 17 - Zr 60,000 25,000 30 - VA tV 36,000 24,000 43 >10 P 34,000 13,000 25 M00 VIB & 4,400 1,900 28 1 VIIB Mn 4,000 1,500 20 1 VIII Fe 45,000 25,000 40 2.3c Co 1,500 700 30 >1 Cu 30,000 6,000 13 1.3c Ni 5,000 3,000 39 2.7c "Values based on an average conversion factor of 50 percent for carbon and published concentration factors of phytoplankton and zooplankton; calculations based on the assumption that the total element is derived from food. 6Schutz and Turekian (1965a) (area of high production). CHighest reported value; other reports indicate no change with depth. ^Structural elements. Relative Uptake of Radionuclides by Zooplankton from Food and Water The calculation of conversion factors in zooplankton from concentration factors is based on the assumption that the zooplankton receive a major part of their trace elements and corresponding radionuclides from food. Not all investi- gators agree with this assumption. According to Polikarpov (1966), The amount of radionuclide transmitted from phytoplank- ton to zooplankton is a function of phytoplankton biomass. When this biomass is many orders in excess of the natural levels, the zooplankton may concentrate more radionuclide from the phytoplankton than directly from sea water. With the normal biomasses characteristic of seas, the quantity of radionuclides concentrated from the water is far in excess of the same radionuclides absorbed from food. Polikarpov further wrote, The pattern that emerges of the ways in which marine ani- mals concentrate chemical elements is, therefore, as follows. The animals satisfy their requirements for most elements by direct absorption from the surrounding water. Intricate organic substances, on the other hand, are usually derived by the animals in the process of heterotrophic nutrition, i.e., at the expense of other organisms. The main source of carbon for the animals is, apparently, to be found in the food links. A certain amount of phosphorus and trace ele- ments incorporated in specific biologically active molecules is also apparently derived in this manner, although it is also possible that there may be direct utilization of such mole- cules present in sea water as a result of their release by liv- ing marine plants. The greater part of the chemical mineral substances and, therefore, by far the greater part of the cor- responding radionuclides are consequently accumulated by marine animals other than with their food. The statement that marine animals reject trace elements in their food but accumulate carbon compounds from this source while taking trace elements through the integument

180 Radioactivity in the Marine Environment from a relatively dilute solution is not consistent with the normal metabolic characteristics of animals studied thus far. Osterberg et al. (1963), in field studies, observed that sur- face adsorption played a relatively insignificant part in the accumulation of 65Zn, 95Zr, 103Ru, 106Ru, 51Cr, and 144Ce in copepods, euphausids, and salps. In laboratory studies, Rice (1963) observed thatArtemia salina concen- trated approximately seven times as much 65Zn from food as from water when the concentration of introduced 65Zn was the same in each experiment. The degree to which a trace element or radionuclide is accumulated from the food or from the surrounding water appears to depend upon the relative concentrations of the element in the two sources. Food in which an element is concentrated only slightly over the concentration in seawater supplies a relatively low frac- tion of the element.* However, when the element is highly concentrated in the food, compared to seawater, a major fraction of the element may be derived from the food through the gut. It is significant that all of the experiments quoted by Polikarpov supporting the concept of direct uptake of radionuclides from seawater (in which the radionuclides were identified) were concerned with uptake of elements for which low concentration factors exist in the food orga- nism. Uptake of this group of elements directly from the water could, indeed, occur. In the case of 90Sr, an average concentration factor of about 20 in phytoplankton and 30 in zooplankton may be derived (Vinogradova and Koval'skiy, 1962;Chipmaner0/., 1958). If azooplankter consumed daily an amount of food equal to 0.3 times its body weight and utilized 85 percent of the contained 90Sr (Table 5) it would have to extract all of the dissolved 90Sr in a volume of water about 5 times (20X0.3 X0.85) its body volume every 24 hours to obtain an equal amount of 90Sr from the water. A medium-sized copepod (Calanus) 2 mm in length can graze the phytoplankton from a volume of water about 500 times its body volume (Cushing, 1959). Its oxygen requirements may be met, however, by the extrac- tion of the gas from a volume of water 20 to 25 times its body volume.t Direct uptake of oxygen and ions from the water probably occurs mainly through mucous absorption, and the volume of water stripped of 90Sr would more nearly approximate that stripped of oxygen rather than of *Food organisms may have high concentration factors for a radio- nuclide yet contain small amounts at any given time because they are not at equilibrium with the radionuclide in the water. If the food organisms live in an area of rapid dilution or if they continue to grow rapidly after a single exposure to the radionuclide, they will contain a relatively small amount of the contaminant. tA Calanus 2 mm in length has a body volume of about 0.16 mm3. One zooplankter requires about 0.8 Ml of O2 per hour, or about 19 ul per day (Marshall and Orr, 1955). At 20°C, this amount of oxygen could be extracted from about 3.6 mm3 of air-saturated water per day, a volume 20 to 25 times the volume of the organism. food. Under these conditions, 80 percent or more of the total 90Sr accumulated by the zooplankton would be ac- cumulated directly from the water, and 20 percent or less, from the food. Those elements that are highly concentrated by both marine phytoplankton and zooplankton are not, however, accumulated directly from seawater but, rather, are incor- porated from ingested food. The accumulation of 95Zr by phytoplankton and its transfer to zooplankton may be used as an example. The average concentration factor for 95Zr in phytoplankton is about 60,000, and in zooplankton, about 25,000. Zooplankton appear to convert about 30 percent of the 95Zr associated with the phytoplankton eaten for food. If a zooplankter consumed daily an amount of food equal to 0.3 times its body weight and converted about 30 percent of the contained 95Zr, it would have to extract all of the radionuclide present in a volume of water about 5,500 times its body volume (60,000X0.3 X0.3) each day to obtain an equal amount of 95Zr from the water. If the zooplankter is capable of extracting daily the element from a volume of water only 20 to 25 times its body volume, then 99 percent, or more, of the 95Zr would be accumu- lated from the food. Transport by Zooplankton, Fecal Pellets, Moults, and Dead Organisms Calculations may be made to determine the relative roles of diurnal vertical migration, fecal pellet production, moulting, and death upon the transport of radionuclides. These may be made by using the data of Kuenzler (1965, 1969) on plankton distribution, turnover rates, and percent particu- late excretion, along with other estimates on biological parameters. These include average feeding rates (0.3 X body weight/day), food utilization (50 percent of carbon intake), and the conversion factors, relative to carbon, for the trace elements shown in Table 5. A simplified block diagram for downward transport of iron by biological mechanisms is shown in Figure 4. About 92 percent of 55Fe or 59Fe transported through the ther- mocline by biological mechanisms would be transferred by the influence of gravity on fecal pellets, moults, and dead organisms. Only 8 percent of the element would be trans- ported by vertical migration of the animals. It is difficult to distinguish between direct biological transfer, resulting from exchange of surface-adsorbed material plus excretion of soluble and particulate products of metabolism, and in- direct transfer, resulting from fecal pellets and moults. Varying amounts of excreted metabolic by-products may be associated with voided pellets, and surface-adsorbed matter is lost from the organisms through moulted exoskeletons (Jerde and Lasker, 1966; Fowler and Small, 1968). After equilibration of differences in chemical and physi-

Accumulation and Redistribution of Radionuclides by Marine Organisms 181 UPPER MIXED LAYER MIGRATING ZOOPLANKT0N 1.64 g of animals/m2 in top 100 m 0.246 g of phytoplankton eaten/day in upper mixed layer 0.246 X 135* = 33.2 ^g Fe ingested/day 0.123gof zooplankton synthesized/dayt 0.123 X 75J = 9.2 fig Fe incorporated into zoop1ankton/day 33.2 - 9.2 = 24 ^g of Fe voided or lost from dead organisms/day THERMO. CLINE Biological transport 9.2 fig Fe/mVday DEEP WATER NONMIGRATING ZOOPLANKTON 2.32 g of animals/m2 in top 100 m 0.69 g of phytop1ankton eaten/day in the upper mixed layer 0.696 X 135* = 94 fig Fe ingested/day 0.348 g of zooplankton synthesized/day* 0.348 X 75J = 26.1 fig Fe incorporated into the zooplankton/day 94 - 26 = 68 fig of Fe voided or 1ost from dead organisms/day Biological transport 9.2 fig Fe/m2/day 26 fig Fe excreted. 13 fig pan1cu1ate, 13 fig solution § MIGRATING Z00PLANKTON 1.64 g of animals/m2 0.24 g of phytoplankton eaten/day below the mixed layer 0.246 X 135* = 33.2 fig Fe ingested/day 0.123 g of zooplankton synthesized/day* 0.123 X 75J = 9.2 fig Fe incorporated into zoop1ankton/day 33.2 - 9.2 = 24 fig of Fe voided or lost from dead organisms/day 9.2 fig Fe/m2/day transported out of mixed 1ayer by vertical migration 24 -• 13 -« 68 -* 105 fig Fe/m2/day transported out of mixed layer by fecal pellets, dead animals, and particulate excretion •135 fig Fe/gphytop1ankton. +Based on 50% eonversion of food by zoop1ankton. J75 vl Fe/g zoop1ankton §50% of excreted iron particu1ate, 50% so1ub1e (Kuenz1er, 1965). FIGURE 4 Block diagram showing the downward transport of iron by biological mechanisms in phy- toplankton and zooplankton in the northeastern Pacific (plankton populations based on Kuenzler, 1965). Iron content i n seawater = 3 X103 Mg/m 3 = 3 X105 Mg/100 m 3. Transport of iron out of mixed layer by vertical migration , 3X103 9.2 : 3.26 X104 days = 89 yr. Transport of iron out of mixed layer by fecal pellets, excretion, and dead organisms : 2.86 X 103 days = 7.8 yr. Transport of iron out of mixed layer by all biological processes = 3X103 105 3X103 114.2 = 2.63 X103 days = 7.2 yr. The mean residence time of 90Sr in upper 300 m of the Pacific is 2.7 years (Saiki, 1968). Strontium- 90 is not biologically active, and main transport downward is by physical processes. Transport down by biological mechanism is less than by physical factors. Physical half-life of "Fe is 2.9 yr. In the time required to transport S^K. out of the mixed layer by all biological mechanisms (7.2 yr), the 55Fe would decay to about 18 percent of its original activity.

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Accumulation and Redistribution of Radionuclides by Marine Organisms 183 cal form between the introduced material and that already present in the water, radionuclides of iron would be trans- ported downward by biological processes at the same rate as the normally occurring stable element. The total rate of biological transport out of the mixed layer would be 114 /ug/day/m2 under the specified conditions. The total amount of iron in the mixed layer is 3 X10s /ug/100 m3 (3 X10s jug/m2 for a layer 100 m thick). Transport of iron out of the mixed layer by biological mechanisms would require 3X10s/114+ 2.6X103 days, or 7.2 years. This calculation is based on the assumption that a shear zone exists at the upper edge of the thermocline so that the radionuclides are not transported back into the mixed layer again. Maximum biological transfer is considered to occur, since the assump- tion is made that redissolution of the radionuclides from pellets or dead organisms does not take place in the mixed layer. The time of 7.2 years for biological transport of 55Fe or 59Fe from the surface waters appears to be relatively long in comparison with physical transport. Strontium is subject to little biological transport, and the residence time for90Sr in the top 300 m of the Pacific Ocean is about 2.7 years (Saiki, 1968). Rama et al. (1961) reported a residence time for 210Pb in the upper mixed layer of less than 2 years and proposed that the short residence time was due to vertical biological transport. Goldberg (1965) later reported a resi- dence time for lead of 7 years in the upper mixed layer, based on a nonsteady state for stable lead. In the present calculations, the length of time required for 210Pb (or stable lead) to be transported out of the mixed layer by biological activity is about 7.3 years (Table 6)-about the same as for iron. These values are for a relatively productive area of the sea, however, and the average for the entire Pacific Ocean should be less. The calculations made for biological transport of iron from the upper mixed layer in the eastern North Pacific may be repeated for other elements and radionuclides and for other areas of the sea. The calculations for the times, in years, required to transport 54Mn, 55Fe, 59Fe, 57Co, 58Co, 60Co, 65Zn, 95Zr, and 210Pb from the mixed layer are shown in Table 6 for the eastern North Pacific, coastal areas, and upwelling sites. The areas of the sea considered here represent a wide range of biological productivity with a relatively low standing crop of zooplankton in the eastern North Pacific (0.04 cc/m3), intermediate amounts in the coastal regions (0.44 cc/m3), and high amounts in areas of upwelling (1 cc/m3). According to these data, biological activity would have little effect upon vertical distribution in the open sea. However, the total biological activity of zooplankton could increase the transport of the radionu- clides of iron, zirconium, lead, and perhaps zinc into the deeper waters from the surface downcurrent from areas of high coastal productivity and areas of upwelling. Manganese-54,55Fe, 59Fe, "Co, 58Fe, 60Fe, and 65Zn represent elements that are biologically important as con- stituents of enzymes, vitamins, and molecules that partici- pate in oxygen and electron transport. Of these radionu- clides, those of cobalt appear to be subjected to the least biological transport. This is due mainly to relatively low concentration factors in both the phytoplankton and zoo- plankton. According to the present calculations, the time required for all biological mechanisms to remove the cobalt radioisotopes from the surface mixed layer into the deeper waters of the eastern North Pacific is 240 years, a relatively long time in comparison with the physical half-life of 60Co (5.26 years)-the longest half-life for any of the cobalt radionuclides. Kuenzler (1965) calculated that biological processes would require about 350 years for transport out of the mixed layer but proposed that this transport time might be high by a factor of at least ten as a result of sev- eral biological factors. In the present work, estimates for the removal of cobalt radionuclides from the mixed layer by total biological action of the zooplankton—for coastal areas 20 years and for areas of upwelling 8.8 years (Table 6)—more nearly agree with the low value of 35 years calculated by Kuenzler. Conversion factors for Ag, Zn, Sc, Y, Ce, Si, Sn, Pb, Zr, P, Cr, Mn, and Fe are 40 percent or less, and these elements (or their radionuclides) would be excreted in higher propor- tions than the organic matter. Those elements that are rela- tively insoluble in seawater or form insoluble salts would be retained to a high degree in the fecal pellets. The proposal here that the effect of gravity on fecal pel- lets constitutes a major biological mechanism for the trans- port of some radionuclides and trace elements to the deeper waters from the surface is not new. Rex and Goldberg (1958) suggested that the accumulation of micron-size par- ticles of terrigenous quartz into fecal pellets by filter- feeding zooplankton might provide a mechanism for the rapid transport of this material to the bottom sediments. Goldberg and Arrhenius (1958) found barite (barium sul- fate) in bottom aggregates that they assumed to be fecal pellets of benthic organisms, and Chow and Goldberg (1960) proposed that the increase in barium with depth in the sea resulted from a high concentration of sulfate ions resulting from bacterial decomposition of detrital organic material, which caused barium sulfate to precipitate. Goldberg (1965) stated "barytes crystals, incorporated in, and sinking with, the decomposing organic matter, may either dissolve in deeper waters during the destruction of their carbonaceous matrix or be incorporated in the sedi- ments on the sea floor." Such a mechanism explains not only the depth profiles of barium, but also the observation that sediments below zones of high organic productivity are enriched with barium. This is also true for deposits con- taining large numbers of diatom frustules (Goldberg, 1958). Brongersma-Sanders (1967) demonstrated that at least two species of diatoms concentrate large amounts of barium.

184 Radioactivity in the Marine Environment The siliceous frustules of these species are not preserved in the sediments, but they may act as transport packages to deeper water for barium (Turekian, 1968) and silica, espe- cially if incorporated into fecal pellets which contain rela- tively large amounts of sulfate. Goldberg (1965) proposed that two biological mecha- nisms for transport downward of Hg, rare earths, and 210Pb were likely to exert significant effects. One of these de- pended upon the enrichment of the elements in the bio- sphere with subsequent sinking and continued oxidation of dead organisms and metabolic waste products (including fecal pellets). The other process involved the adsorption of the dissolved metals onto disorganized masses of organic matter with a resulting net transfer from the surface to deeper waters. In both processes, the fecal pellets could play an important role, since they are produced in relatively large amounts, contain significant fractions of the ingested elements, and provide reactive surfaces. Conover (1964) suggested that Calanus hyperboreus contributed largely to the food supply of deeper dwelling animals by producing fecal pellets containing at least 50 percent of the energy originally available in the phytoplankton. Johannes and Satomi (1966) proposed that a significant fraction of the energy contained in marine communities was channeled into the production of fecal pellets and that the quantitative sinking of this material out of the euphotic zone would re- sult in rapid transport of large quantities of phosphate into the deeper waters, provided the element was not rapidly re- dissolved from the pellets. They also postulated that the rate of downward transport of phosphate would be reduced if fecal pellets were utilized by other zooplankton. If this is correct, however, the original fecal pellets would be rela- tively enriched in phosphorus in comparison with the phy- toplankton food (based on transfer of carbon) and the fecal pellets of the omnivores would be further enriched in phosphorus, since the conversion factor for phosphorus in zooplankton is about one half that for carbon (Table 5). Osterberg et al. (1963) presented convincing evidence that some artificial radionuclides are removed from surface waters of the sea to the bottom by fecal pellet production. Samples of sea cucumbers were collected from the bottom at 200-m and 2,800-m depths off the Oregon coast and analyzed for radionuclides by gamma spectrometry. The relative amounts of 144Ce-144Pr, 95Zr, 65Zn, and 40K in the samples from the two depths were used to calculate that the 144Ce-144Pr and 95Zr-95Nb were transported to a depth of 2,800 m in 7 to 12 days but that 65Zn was subject to only limited downward movement below 200 m. Osterberg and his associates noted that the particle sizes of particulate fallout radionuclides were too small to be trans- ported per se to the bottom at the observed rates but that these nuclides were known to be accumulated by herbiv- orous zooplankton from contaminated phytoplankton. The conversion rates for 144Ce-144Pr and 95Zr-95Nb are low in zooplankton, and the authors proposed that the unassimi- lated radionuclides would be released in fecal pellets that would sink rapidly because of their relatively large size. The fecal pellets ofEuphausia paciflca, produced by feeding the diatom Skeletonema costatum to the euphausid, were found by one of the authors to sink at a rate of 43 m per day. Radionuclides associated with fecal pellets sinking at this rate would be carried to a depth of 2,800 m in about 65 days. Elements incorporated onto or into fecal material would be efficiently transported downward and released into the deep waters or the bottom sediments only if they were re- leased from the pellets at a slow rate during descent. In general, elements must remain in particulate or colloidal form for continued association with fecal pellets. Radio- nuclides that would be expected to remain with the pellets would include those that Form relatively insoluble salts or hydroxides in seawater and are accompanied by carrier amounts of similar or the corresponding stable element Form strong complexes with biological surfaces Coprecipitate with inorganic scavengers Are incorporated into biological structural compounds, i.e., the incorporation of carbon, hydrogen, nitrogen, sulfur, phosphorus, calcium, and silica into skeletal material, lipids, proteins, and polymerized carbohydrates. Vertical Distributions of Trace Elements and Radionuclides Distribution patterns with depth of water for several ele- ments and radionuclides determined by different authors are shown in Figure 5. Of these elements, silicon, phospho- rus, nitrate, barium, radium, lead, cerium, neodymium, and total rare earths have been observed to increase in amount with depth even in areas of low biological productivity. Silver, in contrast, shows increased amounts with depth only in areas of relatively high productivity. The structural elements P, N, and Si increase more or less continuously with depth, even in areas of low productivity, down to about 1,000 m, below which little or no increase occurs to 4,000 m. The break at 1,000 m for silicon is not as pronounced as for phosphorus and nitrate, however, and the shape of the distribution curve for silicon appears to be intermediate between the structural elements and those in the next group. The elements radium, lead (210Pb), barium, cerium, neodymium, and the total rare earths* increase slowly in amount down to a depth of about 600 m, with a rapid increase in amounts between 800 m and 1,000 m. *Only two values were given by Goldberg and Koide (1963) for the total rare earths (surface and 4,000 m); however, these points both fall near the curve for barium.

Accumulation and Redistribution of Radionuclides by Marine Organisms 185 1000 3000 4000 400O IO 12 14 16 18 20 22 46OO1 1 1 ' ' ' ' ' ' I '—L 6 8 10 12 0 10 20 S0 40 S0 60 70 80 90 10OIIO 120 FIGURE 5 Distribution of Si, P, N, Ag, Ce, Ra, Nd, 210Pb, Ba, Y, and Sc in water with depth. Ba- Chowand Goldberg (1960); RE (rare earth)-Goldberg and Koide (1963); 210Pb-Rama et al. (1961); Ag-Turekian and Schutz (1965a); Ce, Nd, Y, and Sc-Hogdahl et al. (1968); Si, P, and NO3, average of Pacific, Atlantic and Indian Oceans- Sverdru pet al. (1942). Below 1,000 m, the amounts of the elements in the water increase slowly down to a depth of at least 4,000 m at about the same rate as that above 800 m. All of the elements and radionuclides in which transport by fecal pellets, moults, and dead organisms (Table 7) constitutes 99 percent or more of the total biological trans- port show strong increases in amounts in the water with increased depth. These include silicon, barium, rare earths, and lead. Silver, on the basis of concentration factors in phytoplankton and zooplankton, would be transported only about 91 percent by fecal pellets, moults, and dead organisms, yet it appears to have a vertical distribution pat- tern in areas of upwelling similar to the elements listed above. Schutz and Turekian (1965a) attributed the increase in silver with depth to downward biological transport and regeneration of silver in the deeper waters. This metal is known to be concentrated highly in the digestive glands of crustacea (Palumbo, personal communication, 1959; Seymour, 1963; Folsom and Young, 1965), although it is concentrated only slightly in other tissues of these orga- nisms (Zesenko, 1965;Lowmanef a/., 1967b). Although cerium is transported 99 percent or more by fecal pellets, moults, and dead organisms, its distribution pattern does not conform to that expected from the calcu- lated time (2.9 years) to transport the element out of the upper mixed layer by biological action in areas of high pro- ductivity. The vertical distribution of the rare earths (Goldberg and Koide, 1963) in the open sea and the observa- tions of Osterberg et al. (1963) on the presence of 144Ce- 144Pr in sea cucumbers at 2,800 m off the coast of Oregon indicate that the rate of downward transport is much greater than that calculated. The long transport time re- ported here appears to result from the low concentration factor used for phytoplankton (4,000), based on laboratory uptake experiments (Chipman, 1958). If this concentration factor occurs under field conditions, then the zooplankton must ingest significant amounts of cerium from sources other than phytoplankton, or stable and radioactive cerium must be adsorbed directly onto fecal pellets and other biological debris, including dead organisms, in amounts greater than those accumulated by the phytoplankton. Data to resolve this question are not available at the present time, although it is known that cerium shows a marked propensity for adsorbing onto surfaces, both organic and inorganic. The similarity in vertical distribution patterns of phos- phorus and nitrate is probably due to their being incorpo- rated into structural compounds of phytoplankton with approximately equal concentration factors and to both being released from structural biological material through breakdown by bacteria. Although bacteria would also de- compose the protective layer covering the frustules of diatoms (Cooper, 1952; Lewin, 1961), the release of silica, per se, would result from ordinary inorganic re-solution of the silica tests and not from decomposition by bacterial oxidation. Iron, copper, zinc, cobalt, manganese, and, perhaps, nickel are associated with organisms as constituents of re- active biological molecules. These catalyst elements occur both in plants and animals, and, except zinc, all are mem- bers of the first series of transition elements, which form essentially covalent linkages as well as ionic complexes.

186 Radioactivity in the Marine Environment In general, the catalyst elements are not as firmly incor- porated into biological structural material as are the struc- tural elements carbon, hydrogen, nitrogen, and phosphorus. Some chelates of copper and iron exist as hemes, however, which are extremely stable, although they are associated with free erythrocytes or are in solution in the blood of marine animals. Cobalt is an integral part of vitamin B12 that appears to be extremely stable in the marine environ- ment. Other chelate complexes with transition elements are not as stable as the hemes and B12, and in some enzymes the metal-protein complex is less stable than the metal-free protein (Lehninger, 1950). In addition to their being incorporated into biological catalysts, the transition elements and zinc are also capable of forming complexes with biological surfaces so that ap- preciable amounts of these elements associated with marine organisms may not be incorporated into the organisms but only adsorbed onto surfaces. Thus, Wolfe (1970) estimated that as much as 96 percent of the total zinc in the oyster Crassostrea virginica was not incorporated into physiologi- cally important molecules but was loosely bound to cellular components from which it could be removed by dialysis without impeding the zinc-dependent enzyme action of alkaline phosphatase. As a consequence of the lower degree of stability of complexes between such loosely bound ele- ments and the biota, compared to incorporated structural elements, they would be expected to be remineralized rap- idly from organic detritus, including fecal pellets and moults (Fowler and Small, 1968) and from dead organisms more rapidly than the integrally combined structural elements or those elements forming insoluble salts or hydroxides in seawater. Conflicting observations have been made on the depth distribution of iron, nickel, copper, and zinc in the sea. Corcoran and Alexander (1964) measured the amounts of nickel, iron, and copper in the Atlantic Ocean off Florida and observed increases with depth. However, in a later study of the area, they found a reverse distribution for copper, with the metal occurring in slightly greater amounts in the surface waters than at depths down to 800 m (Alexander and Corcoran, 1967). No correlation was found between phytoplankton (based on chlorophyll A) and copper levels. Schutz and Turekian (1965a) observed increases in concen- tration with depth for silver and cobalt in three out of four areas of high productivity (upwelling) but did not find sig- nificant increases in nickel. Morita (1955) found that the deeper waters of two deep bays in Japan were slightly en- riched in copper and zinc, although the differences from surface values were not great. Slowey (1966) reported that the distribution patterns of copper and zinc were similar off the Pacific Coast of South America but were different from that of manganese. The rates of biological transport for zinc and copper are similar and are about six times that for man- ganese (Table 7); thus, the difference in distribution pattern would be expected. Along the west coast of South America, Slowey (1966) observed that the greatest amounts of cop- per and zinc were found in areas of upwelling and high bio- logical productivity. Upwelling areas may provide sinks for biologically important elements. Because surface currents transport phytoplankton and zooplankton downwind from TABLE 7 Calculations of Transport of Trace Elements and Radionuclides Downward by Vertical Diurnal Migration of Zooplankton and by Sinking of Fecal Pellets, Moults, and Dead Animals and Time Required for Zooplankton to Transport Radionuclides, Introduced at the Surface, out of the Upper Mixed Layer" Percent of Vertical Transport by Zooplankton Time in Years to Transport Element out of the Mixed Zone by Biological Processes6 Radionuclide Diurnal Vertical Migration Fecal Pellets, Moults, and Dead Animals Eastern North Pacific Upwelling Areas 14C 12 88 94 3.8 32p 6 94 9.6 0.4 Si <1 >99 17 0.7 54Mn 5 95 74 3 55Fe 8 92 7.2 0.3 60Co 7 93 220 8.8 Ni 9 91 66 2.6 64Cu 3 97 11 0.4 65Zn 4 96 12 0.5 95Zr 6 94 5.4 0.2 n0Ag 9 91 11 0.4 140Ba <1 >99 17 0.7 144Ce <1 >99 73 2.9 210pb <1 >99 7.3 0.3 "See Figure 4 for method of calculation. hl IIK.S not include transport by sinking of dead phytoplankton.

Accumulation and Redistribution of Radionuclides by Marine Organisms 187 the areas of high productivity, a continuing downward rain of organic debris would pass out of the upper mixed layer through a shear zone into the deeper layers of water return- ing toward the areas of upwelling. With the trapping of the biologically incorporated elements in the system and the continued addition from incoming deeper water, the ele- ments may build up to levels several times those found in the open sea. Menzel and Spaeth (1962) were unable to demonstrate that more iron was present in the deeper waters of the Sargasso Sea than in the surface layers. In areas of high biological productivity, however, the distribution patterns of iron, nickel, copper, zinc, and silver appear to be related to biological activity. Menzel and Ryther (1961) showed that iron was a limiting factor in the growth rate of phy to- plankton in the Sargasso Sea, an area of relatively low productivity, although the plants did not effect a change in vertical distribution of the element. Menzel and Spaeth (1962) also did not find a seasonal cycle for iron in the Sargasso Sea, but Thompson and Bremner (1935) and Armstrong (1957) found marked seasonal variations of iron in Puget Sound and the English Channel, respectively. Seiwell (1935) observed total depletion of iron in the sur- face waters of the Gulf of Maine during August, although the metal was present in the waters below a depth of 40 m. Raymont (1963) stated that the reduction of iron in the upper layers might, at times, become temporarily limiting. Thus, the vertical distribution patterns of the catalyst elements appear to be significantly influenced by biological action only in areas of high productivity and high density of organisms-usually near land masses with upwelling or addi- tion of nutrients from runoff of surface water. Biological influence upon phosphorus, nitrogen, silica, radium, lead, barium, and the rare earths would also be greatest in these regions. The radionuclides considered in Tables 2 and 3 whose distribution patterns may be influenced by biological activity in marine areas of high productivity include 144Ce- 144Pr 2ioPb noAg 65Zn, ssFe, and 59Fe The radio. nuclides 32P (half-life 14.3 days) and 95Zr (half-life 65 days) would not be subject to significant biological transfer because of their short physical half-lives. Another radio- nuclide, 226Ra, occurs naturally and has a long physical half-life. Although this element is used in medicine, indus- try, and research, its large-scale introduction into the sea by man does not appear likely. ESTUARIES Characteristics Estuaries, salt marshes, bays, sounds, and shore lagoons lie geographically, geochemically, and biologically between the terrestrial and marine hydrospheres. They have highly di- verse physical, chemical, and biological characteristics that affect the distribution and transport of trace elements and radionuclides. These characteristics include depth; width and shape of submerged areas; seasonal and daily changes in sunlight and water temperature; rate of evaporation; height of tidal excursion and strength of tidal bores; geological substrates of neighboring watersheds and rate of addition of river colloids, dissolved ions, and suspended sediments; wind direction and velocity; strength and direction of adjacent ocean currents; and the rate of exchange of estuarine water with that of the open sea. Estuaries may be broadly divided into marine-dominated, river-dominated, and evaporate categories (Wood, 1965). Because of the diversity exhibited by estuarine environments, all types cannot be considered individually in this discussion; however, the more important characteristics of estuaries that influence the interaction of the biota with added trace elements or radionuclides will be reviewed. Influence of Sedimentation upon Biological Availability of Radionuclides Estuarine areas differ from the open sea in several features that alter the relative influence of the water, organisms, and bottom sediments upon trace element and radionuclide transport and distribution in the two environments. In the sea, limited sedimentation processes are slow, and the depth-solubility relationships for elements in the deeper waters plus the length of time required for particles to sink to the bottom result in the return of most elements to the water as ions or colloids before they reach the bottom. In contrast, relatively high rates of sedimentation occur in estuarine areas. Estuarine nutrients are supplied mainly by surface run- off, which leaches organic and inorganic materials from the watersheds. The nutrients are transported by rivers, primar- ily in solution or in colloidal form, although some rivers of high velocity may contain large amounts of suspended sedi- ments, especially during flood conditions. Variable amounts of biologically important elements, including iron, manga- nese, cobalt, zinc, copper, molybdenum, and phosphate, are supplied by the rivers, usually in great excess of the amounts the photosynthetic plants are capable of utilizing or even accumulating. Nitrate is also supplied by rivers, but, unlike the elements listed above, it is usually introduced in small amounts and often may be a limiting factor for organic pro- ductivity in estuarine areas (Ketchum and Bowen, 1958). Other elements with no known biological function may also be supplied in amounts exceeding their solubility in sea- water. These include scandium, silver, zirconium, lead, and cerium (Carpenter and Grant, 1967). When rivers enter estuaries, current velocities decrease, and, as a result, much of the suspended sediments sink at

r~ v> oo o * c) — r- o o 1= 00 O O C3 (X> O o w* to — * ^ c tf N (N 10 fO O O tS C3 Os O C5 O r~ cs : JS VI ~ ca r* 10 O O O 1O O p- O ^j g -s c 1 CO CO ca ri ro• H X ca O -^ rs r~ o rt 'tt O 10 Tf O O os o -H S 0 •o 2 00 (N §sO O ^D O C 6 Os (N O ^L V^ "^ O 1 u 1 o ~ r -H ^H •3 th CO u I* '*-' ca ^H sO fO O rt fO fl O O 5 a > * r- M o »-H C •l o n *N (N 1— 1 ^H = to o oo o ro (N O *N ro o s6 o o — . •* N C 6 •a ca 8 u c * Si r~* as *t CD § * sO rN O O O ^ O e o .o *o *«• m 1 O O 0 i •»* XXX 1 S *-H fO NO Tf ro rN S s Q> -a os a o - e u J S a M CA *- a> *5 S ca .1 1i 1 O ? 1 If .1 1 5 c x '3 *o 8 Distribut; I -s p t i » 1 1 1 11 - 5 * ; i! s? ^ 8 u •o js 1 I 1 •!= S » 1 s g | s £ s.g V bO TABLE 11 •E. ?| & z i rt e J2 ^ 0 *2 *U CO co OH ^ H ff- m C/1 a .o 188

Accumulation and Redistribution of Radionuclides by Marine Organisms 189 rates dependent on the size and mass of the particles. Upon mixing of the river water with the saline waters of the estu- aries, iron, aluminum, gallium, titanium, zirconium, scan- dium, and dissolved silica precipitate into hydrous gels, and the coagulation of colloidal clay particles occurs because of the increase in pH and electrolyte content of the water. Simultaneously with precipitation of these colloids, mag- nesium and calcium may exchange with some, but not all, of the cations adsorbed to the suspended particles of river sediment. Zinc, at least, is not accumulated by Columbia River sediments through a simple ion-exchange reaction. Johnson et al. (1967) observed that only an insignificant fraction of 65Zn (0 to 3.3 percent; average 0.76 percent) was removed from freshwater Columbia River sediments by artificial seawater. In contrast, 0.05 MCuSO4 solution re- moved 33 to 54 percent of the radionuclide. In nine sam- ples of Columbia River sediment, about 40 percent of the 54Mn and none of the 51Cr or 46Sc could be removed by the action of artificial seawater. The authors attributed the behavior of the 65Zn to "specific absorption" (Tiller and Hodgson, 1962), in which the metal sorbed to the sediment cannot be displaced by alkali or alkaline earth metals but may be displaced by other transition elements. The general order of displacement from sediment or soils is Cu+2 > Co.t-2>Zn+2>Mn+2. Precipitation and coprecipitation of river, materials is pri- marily a physicochemical process. The ensuing association of the precipitates with suspended and bottom sediments, detritus, and biota does not result entirely, however, from inorganic mechanisms. For some elements, at least, the bac- teria and other microorganisms associated with the surface of the sediments, detritus, and organisms appear to play a significant role in the adsorption and desorption of fine pre- cipitates and ions from and to estuarine waters. In addition, benthic filter feeders may accelerate sedimentary processes in some areas by producing fecal particulates from ingested colloids and fine particulates (Duke et al., 1966). Estuarine sediments are of primary importance in deter- mining the distribution and availability of added trace ele- ments and radionuclides to the water organisms. This is true because the sediments present the greatest total reactive sur- face of the estuarine components, contain large amounts of adsorbed periphyton, and are subject to gravity. Sedimenta- tion in estuarine regions is highly efficient, with rapid re- moval of most nonconservative elements from the water to the bottom, so that only a minor fraction of this material, introduced by rivers, reaches the open sea. Thus, the sedi- ments retain added trace elements and radionuclides in estuaries so that they are available to organisms for longer periods of time than if the trace elements remained in solu- tion or were suspended in the water. Parker (1962, 1963) and his associates calculated the mass, per square meter, of the water, upper sediments, and organisms in a Texas salt marsh and determined the distribu- tion of available cobalt, iron, manganese, and zinc under equilibrium conditions in the system. With an average water depth of 1 m and a 3-cm depth of sediment available for exchange reactions, the water accounted for almost 97 per- cent of the total mass, the sediments about 3 percent, and the total biomass about 0.35 percent (Table 8). Although the water represented most of the mass, it contained only minor amounts of the four elements, accounting for about 3.1 percent of the cobalt and less than 1 percent of the iron, manganese, or zinc. In the sediments, only extractable or biologically available element contents were considered. Even with this restriction, 70 to 95 percent of the four elements were associated with the sediments. The water-to- sediment ratios were 1/1,000 for iron, 1/550 for manganese, 1/110 for zinc, and 1/24 for cobalt, suggesting that iron and manganese were more strongly influenced by sedimentation processes in this type of estuary than were zinc and cobalt. Turekian and his coworkers (Carr and Turekian, 1961; Turekian and Schutz, 1965; Schutz and Turekian, 1965a and b; Turekian, 1965,1968; Kharkar era/., 1968) consid- ered in detail the removal of trace elements from rivers and seawater in nearshore areas and emphasized the action of the biota in removing added cobalt, nickel, and silver, supplied by streams, to the sediments. Kharkar etal. (1968) studied the adsorption of several elements onto ferric hy- droxide, manganese dioxide, and clays under conditions that simulated the river environment, followed by desorp- tion in seawater. In experiments with freshly precipitated ferric hydroxide, 79 percent of cobalt, 50 percent of silver, and 74 percent of selenium originally dissolved in fresh water remained associated with ferric hydroxide precipi- tated under estuarine conditions. In nature, this reaction could result in significant sedimentation of these three ele- ments. In similar experiments with clay, 27 to 55 percent of cobalt, 14 to 25 percent of silver, and 15 to 35 percent of selenium supplied by the streams would be carried to the bottom sediments by settling clay particles in the marine environment. Manganese hydroxide, in general, was least effective in coprecipitating several trace elements, with 20 percent of total stream cobalt, 4 percent of total stream silver, and 34 percent of total stream selenium re- maining associated with the particles in salt water. Jones (1960), in laboratory experiments with radioru- thenium, observed that the uptake of nitrosyl ruthenium by sediments was directly proportional to their surface areas and that, once adsorbed, less than 7 percent of the ruthe- nium could be removed from the marine sedimentary par- ticles by seawater even at pH values of 6,4, or 2. He observed further that ferric hydroxide was capable of interacting with the radioruthenium and the sediments, enhancing the uptake and retention of the element. Jones reported Where rivers flow to the sea via iron ore deposits, iron is brought to the sea in relatively large quantities particularly as colloidal particles. ... When ferric ions are added to sea water containing (Amersham) nitrosyl Ru106 and shaken

190 Radioactivity in the Marine Environment for six hours, there results an insoluble complex between the iron and ruthenium which can be removed by centrifu- gation. In such an experiment .. . some 70 percent of the Ru106 was removed at an iron concentration of 1 ppm. Jones observed that by doubling the amount of iron nor- mally adsorbed onto the sand fraction of the marine sedi- ment (1.4 mg Fe/g sand to 3.1 mg Fe/g sand), the uptake of 106Ru from seawater also doubled when the sand was subsequently placed in the contaminated seawater. In field studies of the accumulation of nitrosyl ruthenium by fine particles and marine organisms near the outflow of the Windscale Works on the Irish Sea, Jones attributed the major uptake of radioruthenium to physical adsorption. Templeton and Preston (1966) reported that concentration factors for 106Ru in British nearshore sediments, or for suspended matter that later settled out, were largely a func- tion of particle size and ranged from 102 for coarse sands to 104 for finely divided silts. Even in productive areas the top centimeter of bottom sediments may provide a mass three times that of the total biomass (Parker, 1962), and minimum concentration factors of 3 X102 to 3 X104 in the biota would be required to equal physical adsorption by the top centimeter of sediment. Frequent resuspension of the top several centimeters of bottom sediments by wind action and turbulence from tidal currents would increase even more the relative adsorption efficiency of the sediments. Hampson (1967) measured the dispersion of 95Zr and 95Nb in estuarine areas. These elements adsorb strongly to surfaces, in comparison with 106Ru, which represents radio- nuclides of medium adsorptive characteristics. Concentra- tion factors for 95Zr in the sediments varied from 4 X104 to IX 10s andfor95Nb, from 6 X 10s to 8 X 10s, compared with the average activities of the two radionuclides in the water over a 4-week period. These concentration factors were 100 to 200 times as great as those measured in the benthic alga Porphyra for the same radionuclides (CF 95Zr, 410; CF 95Nb, 430), and the higher values measured in the sediments are as great as or greater than any reported for any marine organisms, for 95Zr or 95Nb. According to Hampson, "The high concentrations of 95Zr and 95Nb found on sedi- ments at Dounreay indicate a strong scavenging of these two nuclides from the sea water by siliceous and detrital material."* In addition to the rapid removal of iron, aluminum, silver, cobalt, ruthenium, manganese, scandium, zirco- nium, and niobium to suspended and shallow bottom sediments, other elements, including zinc and phosphorus, are also concentrated by the sediments. Orr (1947) and Marshall and Orr (1948) observed that large amounts of phosphate disappeared from a semi-isolated shallow marine *The conditions quoted by Hampson are for Dounreay. Peculiar to the Dounreay situation is the siliceous and detrital material. Accord- ing to W. L. Templeton (personal communication), these conditions do not exist in the Irish Sea. basin at rates much greater than could result from phyto- plankton production. Bachmann (1963) showed that oxi- dized sediments could remove 96 percent of zinc added to saline waters in 22 days, and Seymour and Lewis (1964) found that 69 percent of 65Zn in the water off the Wash- ington coast in the shallow but open sea areas was associ- ated with particles that were stopped by a 0.45-/u filter. Duke et al. (1966) studied the movement of 65Zn (added to the water in solution) through an estuarine ecosystem con- tained in a walled pond. At the end of 100 days, 99.4 per- cent of the remaining zinc was in the sediments and the associated periphyton, and 0.6 percent was in the plants and animals. Evidence that other elements also precipitate from river water added to shallow areas of the sea has been observed by several investigators. The average scandium content of the leaves of sugar cane is about 4.3X10~2 Mg/g of living leaf. The average scandium content of washed leaf detritus from sugar cane in the top layer of nearshore marine sedi- ments in one bay of Puerto Rico is about 5.2 ng of scandium per gram of wet leaf fragment—an increase of about 120 times that of the content in living material. The iron content in the detritus was about 210 times, nickel 3 times, and manganese 2.2 times the amounts of the same elements in the living leaves (D. K. Phelps, personal communication). This is in agreement with the observation of Hood and Slowey (1963) that a large portion of the manganese in the water of the Brazos River of Texas was deposited quickly in the vicinity of the fresh water-seawater interface and that the manganese was not associated with clay. Manganese is known to be coprecipitated with iron under estuarine conditions. In most cases, the amounts of iron and other easily hy- drolyzed elements in seawater probably do not form pre- cipitates large enough to sink from gravity. A large fraction of these precipitates appear to adsorb rapidly and firmly to the surfaces of mineral and clay particles, to phytoplankton and zooplankton, and to particulate organic detritus. These larger particles are usually subject to sedimentation, the rates dependent upon their size, shape, and specific gravity. In addition, particles as small as bacteria, at least, are sub- ject to efficient removal from the water by benthic mol- luscs, which are capable of essentially complete removal of particulates from volumes of water two orders of magnitude greater than that of the animal volume in a few hours (Lund, 1957a and b). Effects of Epiphyton on Uptake and Loss of Radionuclides by Sediments Relatively few investigations have been made to compare the role of bacteria and of inorganic adsorption processes in the uptake of trace elements and radionuclides by near-

Accumulation and Redistribution of Radionuclides by Marine Organisms 191 shore suspended and bottom sediments. Microbial epiphyton show a marked propensity for association with particulate material and for the accumulation of ionic and colloidal trace elements. They thrive in estuarine areas supplied with organic food and other nutrients from river runoff in which an abundance of surfaces upon which the microbes may flourish are present, in comparison with the situation in the open sea. Marine bacteria appear to require these surfaces for continued growth and division. Rubentschik et al. (1936) reported that bacteria ad- sorbed readily onto positively charged mud particles in saline sediments and that 99.2 percent of all the bacteria were adsorbed to the sediments at an optimum concentra- tion of about 2 cells per microgram of mud.* Wood (1953) observed that optimum bacterial adsorption occurred on particles 1 to 2 n in diameter and that up to 99.8 percent of the cells were adsorbed. The association of periphyton with sediments appears to be directly related to the available ad- sorptive surface area. Thus, greater numbers of microorga- nisms are associated with smaller particles. Wood (1965) showed that the amounts of nitrogen in estuarine sediments increased rapidly with decreased particle size. A significant fraction of total nitrogen in some estuarine regions may be associated with the epiphyton in sediments. According to Wood, the microbiota associated with these fine particles are important in food chains because many animals, includ- ing mullets, are capable of selecting for fine particles. For the large amounts of epiphyton in sediments to sig- nificantly influence the distribution of added trace elements or radionuclides, these organisms must be capable of accu- mulating the contaminants at concentration factors com- parable to those of inorganic adsorptive mechanisms that operate on the sediment surfaces. Marine periphyton are known to accumulate several trace elements efficiently. Chipman and Schommers (1968) cleaned the marine clam Tapes of bacteria and kept it in sterilized seawater. The shells accumulated 1/22 to 1/36 as much 54Mn as the shells with bacteria, although metabolic uptake into the soft parts of the sterilized and unsterilized clams was the same. Lowman et al. (1956) noted that the accumulation of radionuclides by benthic algae at the Eniwetok test site was directly related to surface area of the plants. Several radionuclides, including 65Zn, become rapidly adsorbed to the walls of plastic aquaria containing marine bacteria, although little or no adsorption occurs under sterile conditions. Zobell (1946) pointed out that placing seawater in a container increased the number of bac- teria sharply and unnaturally in comparison with natural conditions. This characteristic of aquarium environments has plagued many investigators studying the uptake of a wide variety of radionuclides by marine organisms. In both fresh and marine water, the periphyton exhibit marked *At this concentration, the sediment/bacteria ratio would be ap- proximately 300/1. ability to accumulate a variety of biologically important radionuclides. However, quantitative measures of concen- tration factors in these organisms are difficult to determine because of their extremely small biomass and their intimate association with the substrate (Kevern et al., 1966). Pomeroy et al. (1967) observed that relatively large amounts of phosphate and trace metals were adsorbed onto the sediments in salt marshes of the eastern United States. According to Pomeroy et al., there is little doubt that the bacteria adsorbed to the sediment particles provided an im- portant link between the adsorbed material on the sedi- ments and filter-feeding and deposit-feeding benthic orga- nisms. Pomeroy and his associates found that 65Zn and 32P, introduced into the estuarine regions, were adsorbed quickly and locally near the sites of introduction and were not transported appreciably by water during short periods of time. Because most of the 65Zn and 32P became adsorbed onto the particles of sediment and detritus, the filter-feeding benthic organisms were the first to show detectable amounts of the radionuclides and to reach peak levels of activity. The turnover times in the filter feeders were long, and these organisms provided a relatively large biomass in the area in- vestigated. Pomeroy et al. postulated that the benthic filter feeders thus provided a pool for slowing the movements of the radionuclides through the system. The 65Zn and 32P reached equilibrium between the water and the sediments within 24 hours. With continued additions of radionuclides, the amounts in the sediments would in- crease until daily loss equaled daily accumulation in the sediments. At equilibrium the amounts in the sediments would greatly exceed the amounts in the water and the amount added each day. Pomeroy et al. did find, however, that continuous exchange occurred between the water and the sediments and that the radionuclides became more widely dispersed with time. Pomeroy et al. (1965) reported that the exchange of phosphate between the water and the sediment was controlled by two mechanisms, one an in- organic sorption reaction and the other controlled by bio- logical exchange, probably between adsorbed microorga- nisms and the water. In surface fractions of the sediments poisoned by formalin, the rate of inorganic exchange of phosphorus was only one half to two thirds the rate of in- organic plus biological exchange for sediments with living microorganisms. If the same fraction of total exchange holds for other elements as for phosphorus, then the micro- organisms may exert a profound effect upon trace element distribution in sediments. Concentration factors in sedi- ments for several nuclides, based on micrograms of ex- changeable iron, manganese, phosphorus, calcium, and strontium per gram in sediment divided by micrograms of element per gram in water (or on activity of radionuclides of zirconium, niobium, and ruthenium per gram in sedi- ment divided by the activity per gram in water), have been reported as follows:

192 Radioactivity in the Marine Environment Nuclide Concentration Factor Reference Fe 2.9 X107 Ganapathy et al. (1968) Mn 2.8 X106 Ganapathy et al. (1968) Nb 6X104 toSXI05 Hampson(1967) Zr 4X104 to IX 10s Hampson(1967) P 7.5 X104 Ganapathy etal.( 1968) Ru 1.0X104 Templeton and Preston (1966) Ca 70 Ganapathy et al. (1968) Sr 33 Ganapathy e? a/. (1968) germanium, arsenic, bromine, molybdenum, iodine, and lead (Chilingar et al, 1967). Keith and Degens (1959) have reviewed the similarity of trace element assemblages in sedi- mentary pyrites and those in organisms and the possibility that the elements were collected by organic material. Arrhenius (1959) discussed the enhanced amounts of zinc, copper, lead, tin, and silver in biogenous apatite, and sev- eral authors have reported positive relationships between biogenic carbon and trace elements in shales (Twenhofel, 1932; Mason, 1958). In the case of iron and manganese, the extremely high concentration factors are most probably due to inorganic precipitation of iron and coprecipitation of manganese. For the other elements, however, a significant fraction of them and their radionuclides may be accumulated in the sediments through biological activity. Even in the case of coral reefs, in which essentially all of the bottom is cal- cium carbonate, only a small fraction of the calcium or strontium in the overlying water is sedimented by biologi- cal mechanisms. Oxidizing Bacteria and Reducing Sediments The combination of precipitation of colloids, physical ad- sorption to sediments, and uptake by periphyton result in large stores of exchangeable nutrients in the bottom sedi- ments. In these shallow areas of high productivity, large populations of oxidizing bacteria often produce reducing environments containing varying amounts of hydrogen sul- fide, especially in areas of limited current and wave action. Ito and Imai (1955) reported that the bottom sediments 300 m distant from Japanese oyster farms contained an average of 0.7 percent total sulfide but that directly under the oyster rafts the sulfide amounted to 4 percent of the total sediments. According to these investigators, "when the bottom sediment is stirred by turbulence, the hydrogen sulfide in the sediment is liberated into sea water. If the oxygen content of the sea water is high, the liberated sul- fide may be left unoxidized." The release of hydrogen sul- fide into the water by resuspension of sediments precipi- tates some of the trace elements introduced into estuaries or sounds (Schutz and Turekian, 1965a). In shallow areas, nickel, copper, zinc, silver, and lead could react with biog- enous hydrogen sulfide in the bottom sediments and be precipitated as sulfides. Evidence that reducing environments and production of hydrogen sulfide are effective in fixing of trace elements in bottom sediments is provided by fossil sediments. Carbo- nate deposits formed in shallow water rich in organic ma- terial often are enriched in vanadium, nickel, copper, zinc, Sedimentation by Benthic Organisms in Estuaries In some estuarine regions, benthic filter feeders may exert profound effects upon the rates of sedimentation. Some of the highest concentration factors for trace elements in ma- rine organisms have been reported for benthic filter feeders. Oysters have been reported to concentrate 65Zn up to 250,000 times the amounts present in water (Chipman et al., 1958; Preston, 1966); however, field experiments of Seymour (1966) showed concentration factors about one order of magnitude lower. These differences in concentra- tion factors are probably due to the fact that uptake in oysters is determined primarily by uptake of particulates from the water and not from the element in solution. Anal- yses of oyster feces and pseudofeces were reported by Haven and Morales-Alamo (1966a), who showed that 70 to 90 percent of the material consisted of illite, chlorite, and mixed-layer clays. Lund (1957a) reported that oysters could clear turbid suspensions of yeast, milk, kaolin, carbon black, fuller's earth, yolk of hen's egg, soluble starch, cal- cium carbonate particles, isolated chloroplasts, Euglena, Chlorella, diatoms, and protozoa. Haven and Morales-Alamo (1966b) observed that the ranges of particle size in feces, pseudofeces, and control sediment particulates were essen- tially the same, with at least 80 percent of the particles under 2 n and 95 percent less than 3 /u. The mineral compo- sitions were similar, with contents of 70 to 90 percent illite, chlorite, and mixed-layer clay. During a 9-month period, the organic content (assuming 40 percent carbon content) averaged 16 percent in the feces, 12 percent in the pseudofeces, and 10 percent in the control sediments. The particulates in the water filtered by the oysters included about equal amounts of bioseston and abioseston. Although some discrimination against the inorganic particulates oc- curred, the composition of the excreta suggest that large amounts of suspended sediments were ingested by the oys- ters. Sediments, with their associated microbiota, were shown above to be capable of concentrating several trace elements at concentrations 104 to 107 over the amounts of trace elements already preconcentrated in the sediments. In addition, bioseston are capable of adsorbing large amounts

Accumulation and Redistribution of Radionuclides by Marine Organisms 193 of hydrous colloids of iron and aluminum along with their suites of coprecipitated metals, and the utilization of these plants for food would contribute greatly to the trace ele- ment accumulation in oysters and other filter feeders. In some estuaries, the molluscs and possibly the barna- cles, tunicates, and zooplankton are more efficient in re- moving phytoplankton, organic detritus, and other small particulates from the water than are the effects of gravity. Many of these organisms select for the smaller particle sizes. J^rgensen and Goldberg (1953) demonstrated that Crassos- trea virginica retained 2- to 3-ju particles, but that a majority of particles smaller than 1 to 2 n passed through the gills and were not utilized. Most of the large particles transported by rivers are dropped near the outflows in which few, if any, filter feeders dwell. Sedimentation of larger sand and silt particles is due almost entirely to gravity. Sedimentation of smaller particles in the l-to-3-ju range often occurs, to a large degree, from the action of filter-feeding benthic organisms-if large numbers of these animals are present. Lund (1957b) showed that the amounts of small particu- lates in seawater that were sedimented through the feces and pseudofeces of oysters in laboratory experiments were eight times greater than those deposited on the bottom by gravity. Haven and Morales-Alamo (1966b) in similar experi- ments arrived at a ratio of 7 to 1 for biodeposition to in- organic sedimentation. Of course, relative sedimentation rates by organisms and by gravity are dependent upon, among other things, the ratio of the volume of water to the volume of organisms. However, several field observations and experimental measurements indicate that in the natural environment, too, biological deposition may sometimes equal or exceed inorganic sedimentation from gravity. In Japan, Ito and Imai (1955) reported that an oyster weighing 90 g (9 g of soft parts) was capable of producing daily a minimum amount of feces equal to 3.3 percent of the live animal weight. At this rate the oyster would pro- duce feces equal to more than 10 times its live body weight per year. These authors calculated that a raft of oysters of 60 m2 would produce annually 0.6 to 1.0 metric tons (dry weight) of fecal pellets, an amount equal to 10 to 16 kg (dry weight) of fecal pellets per m2. The top centimeter of bottom sediment in a square meter weighs about 15 kg; thus, a physical sedimentation rate of about 1 cm per year would be required to equal the biological sedimentation from fecal pellets under the oyster rafts. In a study of biodeposition in the laboratory, Lund (1957b) calculated that oysters covering an acre of estuary bottom would deposit about 7.6 metric tons of fecal ma- terial (dry weight) in 11 days. Assuming that this represents a reasonable average for 9 months of the year, an annual deposition of 190 metric tons would result. An acre con- tains about 4.1 X103 m2. The annual deposit of fecal pellets would thus be 46,500 g/m2. A physical sedimentation rate of about 3 cm per year would be required to equal the bio- logical deposition rate of oysters completely covering the bottom. Oysters could not survive under these conditions, and it appears that the population density of oysters over large areas may be controlled, in part at least, by the pro- duction of excretory products. Even in areas where oysters covered only a third of the bottom, the biological sedimen- tation rates would be high. Haven and Morales-Alamo (1966b) conducted studies on biodeposition by the oyster Crassostrea virginica through- out the year and related variation in fecal production to season. Below 2.8°C during the winter months, measurable amounts of excretory products were not produced. Maxi- mum amounts of feces and pseudofeces were produced during September. These authors stated In the lower York River, commercial oyster growers fre- quently plant to an acre about 250,000 small oysters simi- lar in size to those used in the trough study. From April through October these would deposit about 405 kg (dry weight)/week of solids with a maximum of 981 kg/week; larger oysters would produce greater quantities. During the interval April through October the young oys- ters would deposit about 3 X103 g of excretory products per square meter, equal to about 2 mm of sedimentation per year. Haven and Morales-Alamo noted that Biodeposition rates for other common species of inverte- brates may equal or exceed that of the oysters, and when the abundance of these animals is considered, the magnitude of the process becomes evident. Barnacles literally cover many wharfs and pilings in the intertidal zone as well as rocks and shells on the bottom. Tunicates compete for space on the same objects and many hundreds may be found in 0.1 m2. Soft clams and ribbed mussels occur in the shallow intertidal zone and their densities may be as high as several hundred on a square meter. Biological Productivity and Radionuclide Distribution in Estuaries Photosynthesis in estuarine areas is accomplished by both phytoplankton and benthic plants. The character of the estuarine region determines the relative importance of the different primary producers. In estuaries near Sapelo Island, Georgia, Ragotzkie (1959) reported that phytoplankton provided little or no production but that marsh grass ac- counted for about 80 percent and benthic algae 20 percent of the total. In estuaries near Beaufort, North Carolina, Williams and Murdoch (1966, 1969) reported that phyto- plankton, marsh grass, and eel grass and benthic algae each accounted for about a third of the total productivity. In other estuarine areas, phytoplankton apparently provide almost all of the photosynthetic activity (Ketchum, 1967). In shallow, turbid estuarine areas, a major source of trace elements and radionuclides for higher trophic levels

194 Radioactivity in the Marine Environment appears to be suspended particles of both organic and in- organic origin (Phelps, 1967; Haven and Morales-Alamo, 1966a and b). Thus, in estuarine regions, food webs are probably not as important as they are in the open sea. Sig- nificant processes governing the transport and distribution of introduced contaminants in estuarine regions may be divided into physicochemical and biological categories: Physicochemical Settling of large particles, with "selectively sorbed" radionuclides, as a result of reduced current flow of rivers Precipitation and coprecipitation by hydrous gels Adsorption of gels and coprecipitates onto suspended abioseston, seston, and bottom sediments Biological Adsorption of precipitated colloids and selective accumu- lation of ions by periphyton Sedimentation by planktonic and benthic filter feeders Sulfide precipitation and regeneration by reducing muds from bacterial action Quantitative measurements are not available from which the relative influence of physical and biological mechanisms can be determined for individual radionuclides, although 32P, 54Mn, 55Fe, 59Fe, 58Co, 60Co, 65Zn, 95Zr, 95Nb, 103Ru 106Ru 46Sc 110Agj and 144Ce-144Pr would be rapidly sedimented by precipitation, coprecipitation, and biological activity. Iron and phosphorus would be partially regenerated, at least, under reducing conditions. Importance of Estuarine Regions to Man More detailed and quantitative data are needed to evaluate the physical and biological mechanisms that control the dis- tribution and transport of radionuclides introduced into estuarine areas. Many of these areas are of critical interest to man. The most populated areas of the world are contained in a strip 250 miles wide around the Pacific, Atlantic, and Indian Oceans. Most of the large cities, with their associated indus- tries, are located close to the sea or on rivers that are navi- gable to the sea. Thus, man's major point of contact with the ocean has been and will continue to be in nearshore areas, especially estuaries. The use and incidental produc- tion of radionuclides will continue to increase; some of these isotopes will never reach the open sea but will accu- mulate instead in estuaries. These regions are important to commercial fisheries since they serve as nursery grounds for larval and immature forms. About 65 percent of all the com- mercial fish and shellfish harvested in the United States consists of species that occupy estuarine areas during some phase of their life cycle. Molluscs provide the third most economically valuable fishery in the United States. Because these animals ingest phytoplankton, detritus, and sediment, they are capable of greatly concentrating some radionuclides. They thus may pass relatively large amounts of short-lived nuclides to man, in comparison to the activity that would be accumulated through other food chains or webs in which the food orga- nisms are more selective in their eating habits. The most significant role of estuarine organisms in con- taminated areas is probably that of transporting the radio- active contaminants from the shallow water areas to man. This redistribution of radionuclides may not be significant in terms of the total amounts released into marine areas, but it may occasionally result in the ingestion of undesirable amounts of these nuclides by some individuals eating large amounts of seafood from limited areas over long periods of time. That the return of radionuclides to man does not rep- resent a significant proportion of the total released has been demonstrated by Templeton and Preston (1966). They state that surveys of the seaweed Porphyra umbilicolis, used as food by man, show that the annual quantities of 106Ru reaching the South Wales alga Porphyra represent less than one millionth of the 106Ru discharged. At the present time, no use of marine food is restricted because of contamina- tion by man-made radionuclides. Restrictions upon food items that may be utilized by man from estuarine regions because of contaminants should not be condoned. Rather, an adequate knowledge of the mechanisms controlling the movements and distributions of radioactive and other con- taminants in marine regions must be used to restrict the in- troduction of these materials to levels that may be safely tolerated in these vital and ecologically sensitive areas. SUMMARY A major fraction of the mass and surface area of the biota in the sea is provided by the lower trophic levels of food webs. Biological transport of some trace elements and radio- nuclides has been attributed to these organisms. One reason is that they are capable of concentrating several elements to levels much greater than their concentration levels in the water; in addition, many zooplankton undergo vertical mi- gration and produce detritus in the form of fecal pellets, moults, and carcasses, which sink because of the influence of gravity. Elements that may be significantly concentrated by marine organisms include structural, catalytic, and heavy divalent elements; heavy halogens; and elements easily hydrolyzed at seawater pH. The amounts of the nutrient elements-phosphate, nitrate, and silicate—increase signifi- cantly with increased depth in the sea, in contrast to the

Accumulation and Redistribution of Radionuclides by Marine Organisms 195 amounts of the conservative elements, which change only with salinity. The heavy divalent ions-barium and lead, the rare earths, yttrium, scandium, and silver—follow the distribution pat- terns of the nutrient elements to varying degrees. Considerations related to biomass, feeding rates, conver- sion efficiencies, and migratory habits of zooplankton, as well as the chemical characteristics of the elements of inter- est, suggest that the major downward transport of these elements and radionuclides is effected through the influence of gravity on fecal pellets, moults, and carcasses, with direct biological transport accounting for 10 percent or less of the total movement toward the bottom of the sea. In estuarine and other nearshore marine regions, the bot- tom sediments are close to the sites of photosynthesis and to the sites of the introduction of fallout and terrestrial additions of radionuclides. 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Chapter Eight ECOLOGICAL INTERACTIONS OF MARINE RADIOACTIVITY V. T. Bowen, J. S. Olsen, C. L. Osterberg, J. Ravera Ecology considers organisms not as individuals in isolation but as components of systems that include other organisms- plants, animals, and the host of microorganisms-and in which the interrelatedness of the lives of the component species, and of all with the environment, is the primary problem for exploration. Clearly, the dichotomy between the approaches of this chapter and those of Chapter 7 is arti- ficial at best and unavoidably vague at many points; it has been, however, a curious aspect of the development of radioecology (Morgan, 1960; Schultz and Klement, 1963; Polikarpov, 1966) that it has concentrated on the direct ef- fects of radioactivity on organisms and, in their environ- ments, on the effects of organisms on the distributions of radionuclides, to the very considerable neglect of compa- rable questions in respect to ecosystems. It is our hope in the present chapter to move toward redressing this imbal- ance, at least to the extent of pointing out problems de- serving attention. It should be clearly understood that no parts of the argument to follow are directed toward the view that levels of radioactivity now in the ocean present hazards to any marine species or ecosystems. Furthermore, present licensing procedures will permit the growth of nuclear power for many years to come without approaching the levels of ra- dioactivity introduced into the oceans by weapons testing. The purely homocentric approach to decisions about safe levels of radionuclide concentrations in the oceans is an in- complete one; nevertheless, we know of no evidence that it has not provided for the protection of man and of the food chains of the sea on which he depends for sustenance. We believe that the probably large gene pools of most oceanic species, and their efficient recruitment from oceanic areas, provide oceanic ecosystems with considerable resis- tance in the face of local introductions of radioactivity. Measurable damage to open-ocean ecosystems may well not be encountered except at higher concentrations of radioac- tivity than man could tolerate. Certainly, experience to date suggests that other factors are of far greater concern. The well-being of man, however, depends on the vigor of the complex ecosystems of the sea; prudence, therefore, de- mands our continuing study of oceanic radioecology to search for possible weak links in these chains, where radia- tion stress could be a problem even at comparatively low levels. It is an essential part of marine radioecology research to study the concentration patterns of radionuclides in ma- rine food elements in order to determine how radioactivity can be returned to man. Such studies should always bear in mind the parallel search for problem areas not for man but for the ecosystems themselves. The oceans and seas are characterized by a physical and chemical stability quite unusual elsewhere in the biosphere. An ecological consequence of this stability has been, ap- parently, that ecosystems of the open ocean are responsive to smaller changes in environmental variables than are typi- cally of significance elsewhere. In such a situation, continu- ous measurement of fundamental ecological parameters, 200

Ecological Interactions of Marine Radioactivity 201 e.g., temperature, salinity, pH, turbidity, insolation, O2- tension, and the like, would be an extremely valuable, as well as obvious, approach. It is, however, extremely difficult to avoid influencing the biological system through the very act of making the desired measurements. An instrument array suspended from a float can cause interesting changes in the ecosystem. Fish are attracted to the float, perhaps ini- tially by the shade. Algae and various sessile organisms with planktonic stages settle on the hard surfaces of the instru- ment package. Birds landing on the float add nutrients to the system, enriching it. In response to increased primary productivity, the grazers move in, followed by the predators. Thus, the mere presence of an instrument array alters the community structure of the system being studied. There may indeed be operating in ecology a parallel of the "un- certainty principle" in physics. At least the great demand in the ocean for surfaces upon which to settle is satisfied in part and temporarily by the introduction of instruments, bringing to the community new members who previously found the site an unsatisfactory place to reside. At rates often significant in terms of "station time," comparable and related changes are introduced by the presence of a ship or other platform for scientist observers. In view of this situation, one may hope that the neutral- ity of computer modeling will permit insights to marine eco- systems that are not susceptible to direct observation, much less to experimental manipulation. In the jargon of today, ecology might be viewed as the "systems analysis" approach to the living world; as such, it appears to lend itself well to computer modeling as an ana- lytical tool. Modeling as an analytical technique is relatively new and by no means universally accepted or even under- stood, but we feel it is especially promising for study of marine ecology. ROLES OF MODELS IN THE FUTURE OF MARINE ECOLOGY The preparation of Chapters 11 and 12 of The Effects of A tomic Radiation on Oceanography and Fisheries (National Academy of Sciences-National Research Council, 1957) and the Geneva conferences (United Nations, 1958) stimulated thinking about some of the large-scale problems of the nu- clear age in terms of rather simple mathematical models. It was never expected that models of four mixed "boxes" would encompass all that has been learned about the hydro- sphere, atmosphere, and biosphere in the decade just past. The current chapters on physical circulation, chemistry, and biology all have suggestions for improvement. But revisions might not have come so quickly if a provocative model of some generality had not been set forth, e.g., by Craig (1957a,b;1963). A commentary on modeling and abstraction as part of general scientific method (Levins, 1966) reminds us that we cannot hope to gain maximum generality, reality, and pre- cision at the same time. Fallout from nuclear tests provided a distinct opportunity for gaining more reality in modeling the atmosphere and hydrosphere—for instance, in permitting recognition of the subcompartmentalization of the tropo- sphere and the stratosphere, in forcing attention to the ac- tual scales and modes of interchanges both within and be- tween the atmosphere and hydrosphere, or in providing direct evidence of the existence of short-circuited pathways for movement of surface water to intermediate depths (Reid, 1965; this volume, Chapter 4). The stage for more precision awaits refined instrumentation and analysis and better sam- pling, designed to answer questions about the mechanism and biological significance of physical redistribution of nu- clides. An irritating and often perplexing aspect of the "re- fined instrumentation and better sampling" question is that these qualifications are based—or appear to be based—on interaction between the model and the experimenter; selec- tion of improved versions is one part of the continuing process of revision of model as well as of observations. In a recent meeting on modeling techniques in biological oceanography (Banse and Paulik, 1969), there was general agreement that construction of simulation models has special promise for marine ecology. Although enthusiastic reference was made to the success of models in fishery population dy- namics (where models have been built for tuna, halibut, salmon, and marine mammals, among others, and have been of great importance in resource management), few other ex- amples could be found of successful use of complex ecologi- cal models in biological oceanography. This impression, that "practical science" is well ahead in the use of models, is strengthened by Watt's (1968) exposition of the potentiali- ties and realities of ecological modeling in resource manage- ment. In more theoretical ecology, however, it seems that in the use of models that actively involve organic matter of the biosphere, living and dead, research may be in a stage com- parable with that of box models for the physical world 10 years or more ago. In order to avoid mistakes of expecting too much or too little from the modeling of a very complex process, we may note several valuable rules and phases of abstraction. Early models are very tentative, but should provide a framework for relating many fragments of present knowl- edge. They are broad enough to encompass a variety of spe- cial cases and suggest possibilities for relating these cases to one another, e.g., in an order governed by one or more pa- rameters. The general models may have too few parts to be very realistic, but specific cases may then become differenti- ated by adding (or subtracting) some components and speci- fying reactions that are more comprehensive (e.g., nonlinear) than those first tried.

202 Radioactivity in the Marine Environment Successive approximations are naturally used to focus attention on parameters (transfer rates) that have relatively greatest direct or indirect impact on the rest of the system or on a component of interest (e.g., man, whales). This sen- sitivity analysis often shows that some coefficients can vary widely with relatively unimportant impact, while smaller changes in a key factor have crucial effects. Such findings thus guide continuing research to put more experimental or field effort on certain variables than before. They spur us to pursue aspects of the problem that might have been over- looked or at least postponed. Later refinements, in some cases at least, will permit sound predictions of the effects of disturbances-and of the fate of the disturbing substances-such as from contamina- tion that has not yet occurred and that one hopes may never occur (e.g., thermonuclear war or massive accidental releases of stored wastes). Where releases of radioactivity are antici- pated (as in waste-disposal activities or in some technological uses of nuclear explosives), we expect the prerelease predic- tions to improve the effectiveness of the operation itself, of the postrelease monitoring, and of further scientific research on both effects and dispersal. We discuss below (p. 207) that although stable element ("analytical") concentration ratios must be considered, they offer guides only to the equilib- rium distribution of any radionuclides whose release may be of concern. In most predictive modeling, the transient con- ditions indicated by kinetic models will be of much greater value. (For further discussion, see Chapter 10.) In each stage of modeling it is of the greatest importance that the model structure be examined for uniqueness. In a report highly pertinent to our discussion of species diversity, Cohen (1968) points out that two models, his own (1966) and Mac Arthur's (1957), lead to exactly the same numerical predictions; he then proceeds to outline a third model also leading to the same numerical predictions. As Cohen points out, the moral is that the justification of the model simply by its accounting for available data cannot be an acceptable conclusion: "It is necessary to ask what other explanations are available, to determine how these other explanations differ in their observable implications, and to search for data which could discriminate among the explanations." This caveat applies equally well to examination of the various relations that make up a model: In an attempt to construct a stochastic model of nickel distribution in the Atlantic Ocean, Spencer (1968) found that observed verti- cal profiles of nickel in the South Atlantic could be pre- dicted by his model only by an approximate doubling of the transfer efficiency assigned to organisms of the southern ocean. The trenchancy of this observation is reduced, how- ever, by the observation that much the same effect on the vertical profile would be produced, after examination of the flux of nickel at the water-rock interfaces on the sea floor, by using a different value and sign for the transfer of nickel between water column and bottom. Since writing this, we have seen the suggestion by Bostrom et al. (1969) that nickel is locally supplied at the sea floor. Another and more dangerous aspect of model-making is psychological: that the elegance of a model will so over- whelm its creator as to induce him to assume that any data from the real world not encompassed by his model's predic- tions must necessarily be spurious. Few examples of this can be cited without introduction of invidious overtones; one reasonably neutral example is that of the practice, routine among hydrographers until recently, of drawing smooth curves through vertical profiles of temperature or salinity and of discarding as bad data any points lying well off the smooth curves, on the not unreasonable assumption that sharp discontinuities of density-determining properties of seawater would not occur. In fact, however, the introduction of devices capable of measuring salinity or temperature as continuous functions of depth has revealed many cases of just such sharp discontinuities-many persisting for consid- erable periods (Wooster and Jones, 1966)-and it is now clear that many of the "bad points" of former years were good points. Too slavish adherence to the "smooth-curve" hydrographic model delayed for some years its testing and the discovery that it is a model only partly applicable to the real ocean. Numerous comparable cases could be cited, pointing up how dangerous a bond is created between a model and its progenitor. In fact, as indicated above, a model exists only for the purpose of being changed, and only in this process are models fully used to clarify our understanding of nature. MARINE ECOSYSTEMS Three major classes of marine ecosystems are clearly recog- nizable: pelagic, benthic, and near-shore. Although each is so complex as to be subject to almost infinite subclassifica- tion, each major class has properties that lead to distinctive responses to introduced radioactivity as well as to more basic ecological factors. Some of these properties are sum- marized in Table 1. The major divisions of the marine environment, pelagic and benthic, have subdivisions that are largely a function of water depth. Light intensity decreases rapidly with depth so that most photosynthetic plants are found in near-surface waters in the photic zone. Below the level of light penetra- tion, roughly 50 to 200 m, photosynthesis is not possible. Animals of the aphotic zone must rely on food derived, either directly or indirectly, from primary production in the overlying photic zone. Pelagic animals, both nekton and plankton, are associated with the water, maintaining buoyancy by flotation mecha- nisms or by swimming. Benthic animals are associated with the ocean bottom. The benthic and pelagic regions merge at the edge of the sea, forming the near-shore environments

Ecological Interactions of Marine Radioactivity 203 TABLE 1 Properties of Classes of Marine Ecosystems Relevant to Their Responses to Introduced Radioactivity Property Pelagic: Open Ocean Benthic: Open Ocean Near-Shore: Benthic and Pelagic Adsorptive surfaces Physicochemical stability Productivity Primary nutrients supply Size range of primary producers Size range of herbivores Food chain length range Population mobility Accessibility to man, both exploitation and effects Largely biological Quite stable Only in euphotic-zone plankton Largely by water mixing Mostly microscopic Mostly small Mostly long Maximum-plankton by currents, nekton by swimming Intermediate to minimal Bottom and resuspended sediment Very stable None Not important Moderate Very low-most by larval travel Minimal Bottom, resuspended sediment, and terrigenous detritus Maximum variability Euphotic zone plankton and attached to bottom- generally high Largely from land and bottom Small to very large Moderate to large Short Both high and low Maximal that combine with properties of the other two regions a number of new properties related to proximity to the land surface. In addition to the implications of these properties for the reactions of the various ecosystems to introduced radio- activity, the availability of radioactivity to them may be expected-and has been demonstrated-to be different. Availability is dependent upon two factors: the foci of in- troduction of radioactivity and the physicochemical envi- ronment into which it is introduced. It is possible that the physical and chemical characteristics of radionuclides intro- duced near shore are systematically different from those introduced to the pelagic or to the benthic environments. With the exception of worldwide fallout, radioactive by- products of man's activities have generally been introduced near shore and will probably continue to be; this has obvious economic bases. Even fallout nuclides not strongly fixed by the land surface-as Slowey etal. (1965) have suggested for antimony-125-must be significantly enriched in near-shore waters by land runoff. With the exception of tragic accidents like those of the nuclear submarines Thresher and Scorpion, the open-ocean benthic environments receive radionuclides only as result of geochemical, biological, or hydrodynamic transport through the other environments. Direct waste- disposal to the deep ocean has thus far involved trivial amounts of radioactivity, although the scale of such disposal may increase as near-shore marine areas (such as the North Sea), or land areas, become no longer able to accept the in- creasing volumes of waste produced. In terms of exposure to introductions of artificial radioactivity, then, the rank order of the three environment classes is as follows: near-shore, most frequent and severe; pelagic, next; and benthic, least frequent and least severe. Both benthic and near-shore environments differ from the pelagic in respect to the amounts and kinds of available surfaces. In the benthic and near-shore environments the sediment-water interface plays a major role, and resus- pended bottom materials in both, supplemented by run-off terrigenous materials in the second, ensure that in terms of surfaces of absorption the biota have considerable competi- tion. This is not so in the open-ocean pelagic environment, where, in the illuminated zone, most available surfaces must be biological; at greater depths, the competition must be largely between organisms and biogenous detritus, which is, in turn, food for the organisms. Menzel (1967) has described unexpectedly uniform concentrations (in place and in time) of organic detritus particles in the deep ocean; this has not been confirmed, however, by work of Hobson (1967) or of others. Both Menzel and Hobson tend to conclude that sink- ing of organic detritus particles is almost negligibly slow, leading to the conclusion that their removal by biological processes must be more significant than removal by sinking. This suggests that recycling of organic material is of major importance in the pelagic environment; in other contexts this has been suggested by Ketchum and Bowen (1958) and by Bowen and Sugihara (1965). For surface-active radionu- clide waste or debris, then, the fraction immediately associ- ated with the biota may be expected to be highest in the pelagic, lower in the benthic, and lowest in the near-shore environments; clearly, however, the feeding habits of the biota quickly modify the effect of this immediate distribu- tion, and the detritus feeders and "surface scrapers" preva-

204 Radioactivity in the Marine Environment lent in the near-shore and benthic environments may wholly reverse this order of exposure. That this is an important set of variables in considering effects of radionuclide introduc- tions is emphasized especially by the studies of Mauchline and others (Mauchline, 1963) and of Chesselet and co- workers (Chesselet and Lalou, 1964a, b; 1965a, b) concern- ing the association of fallout or of radionuclide waste with marine suspensoids. Beyond the differences in basic exposure outlined above, one can discern a variety of differences in detail among the various ecosystem classes that will further distinguish their treatment of, and responses to, introduced radioactivity. These differences are discussed in the next three sections. The Pelagic Environment Nektonic animals such as tuna and whales make long migra- tions through different water masses. Since they are strong swimmers, their travels are not dependent on current sys- tems, and they may encounter different levels of radioac- tivity in the water, depending on fallout patterns or on local sources. Thus, they act as averagers, and the levels of radio- activity they contain depend somewhat on their individual histories. It is known that tuna, salmon, and whales, for ex- ample, accumulate 65Zn in passing through waters off the Oregon-Washington coast. A part of the 65Zn, introduced into the Northeast Pacific by the Columbia River, wil1 be carried in the animals, at least for a time, as they travel into 1ess radioactive parts of the ocean. Local sources of radio- activity offer some promise as tags to use in determining migratory patterns of pelagic animals (Osterberg, 1964; Forster, 1968; Kujala etal., 1969; Jennings, 1968). Because strength and size are needed to swim against or through ocean currents, nekton generally have a high ratio of mass to surface area and are therefore relatively ineffi- cient at taking up radionuclides directly from the water. Data are not available for evaluation of the importance to nekton of radionuclide uptake through the gill-surfaces or by drinking. As discussed below (see page 215),Polikarpov's (1966) lines of argument lead one to conclude that for pred- ators or grazers, a more important source of radioactivity is the smaller organisms in their diet. Plankton, on the other hand, are generally regarded as "drifters"-a part of the water mass in which they reside. They may travel long distances by passively moving with a rapid current, or, where water motion is weak, their travels may be quite limited. Certain macroplankton, such as eu- phausiids, are, indeed, fairly capable swimmers, migrating vertically into surface waters at night and into deeper waters during daylight. Thus, the euphausiids may drift in one di- rection at night and in a different direction during the day. Larger plankton, e.g., euphausiids and salps, effectively filter large volumes of water while feeding. Because of their small size, it seems unlikely that fallout particles would be filterable; nevertheless, salps and euphausiids both responded quickly to increased amounts of 95Zr-95Nb after the 1961- 1962 atmospheric nuclear tests (Osterberg, 1962; Osterberg et al., 1963b). Either the particles of 95Zr-95Nb were ad- sorbed on mucous, were directly filtered, or became at- tached to phytoplankton and smaller zooplankton that were eaten. The last seems most probable, although mucous ad- sorption is also a possibility. Since plankton tend to move with the surface waters and equilibrate with them, they can often be used as biological monitors of the radioactivity in their environments. Smaller plankton are particularly quick to equilibrate. Foster and Davis (1955) reported that plankton algae in the Columbia River attained maximum radioactivity within little more than an hour. Probably, as hinted by some of Lowman's data (1960), marine phytoplankton respond equally rapidly, providing an input of radioactivity from the photic zone directly into the herbivores. In general, among organisms inhabiting surface waters exposed to fallout, the smaller ones are the first to reach maximum radioactivity. A time lag occurs before the maxi- mum level of radioactivity is reached by larger organisms farther up the food chain. Animals from deeper waters take even longer (Seymour and Lewis, 1964). For the majority of midwater pelagic animals, however, the delay in reaching maximum radioactivity may not be large, because of vertical migrations of the organisms or of their food; unfortunately, few data bearing on this point are available. The data of Osterberg et al. (1963a) imply that transport of some fallout radionuclides to the bottom is rapid. In Ap- ril 1963, they found 95Zr-95Nb in sea cucumbers (Paelo- patides) from a depth of 2,800 m. Because of the small size of fallout particles, their settling rates would be too slow to account for the radioactivity of the sea cucumbers at this great depth. The authors therefore attributed the increased sinking rates to the processing of fallout radionuclides into fecal pellets by zooplankton, thereby increasing the particle size and the sinking rate. Pearcy and Osterberg (1967) reported that micronekton and macroplankton from middle depths (to 500 m) show the same seasonal cycle of 65Zn as those from surface wa- ters; this cycle is related to the seasonal change in position of the Columbia River plume. Since no apparent lag occurs with depth, they believe that vertical transport of 65Zn is quite rapid. However, only a portion of the 65Zn reaches deep water. Near-Shore Environment The near-shore environment is considerably different from that of the open ocean. Near-shore areas are generally more productive. In shallow seas over the continental shelf, a large

Ecological Interactions of Marine Radioactivity 205 fraction of the water column receives sufficient light to sup- port photosynthesis. Nutrients are abundant, being confined to the system by the proximity of the bottom. The bottom itself is especially rich in biota, nourished by the photic zone just above it. Radioactivity introduced into this environment will be found later in the water, sediment, and biota. The relative abundance of the radionuclide in each compartment de- pends both on the properties of the sediment and the biota and on the specific radionuclide chemistry. Data presented by Seymour and Lewis (1964) and by Osterberg et al. (1963a) show that for demersal fish and some benthic in- vertebrates from near-shore locations, the content of some radionuclides was smaller the greater the depth at which the organism was caught; this effect may be stronger for 65Zn in Columbia River outflow than for several of the abundant nuclides in worldwide fallout. It was noted by Seymour and Lewis, however, that the fish data could be interpreted as showing differences in physiology at different pressures rather than in radionuclide availability. Even in the unusu- ally well surveyed areas of the Columbia River outflow, we rarely, if ever, have enough data to allow full evaluation of all the complexities of ecosystem responses. The behavior of radionuclides is especially complex in near-shore environments for a number of reasons. The affin- ity of the sediment for the radionuclide depends to a large extent on the particle size of the sediment, the amount of organic material present, and the degree of mixing (see Chapter 6). Biological concentration factors of radioisotopes are influenced by the concentrations of their stable counter- parts, and these levels, too, can be highly variable in waters affected by adjacent land masses. In short, the near-shore area is subject to many environmental variables. Benthic Environment The benthic community in deep waters is only slightly less complex. Many animals live on or slightly below the sediment-water interface. A radionuclide introduced into this environment would be subject to sorption on sediment surfaces or to biological uptake. Chesselet and Lalou (1964a, b; 1965a, b) showed that, at least for some elements, the sediments quickly bind most of the radioisotopes. Benthic organisms that ingest sediment particles may or may not re- move the radionuclides from the sediments, depending in part on the pH of their digestive systems. It seems clear that unless plants and animals associated with the sediment- water interface can remove radioactive trace elements from sediment particles, most of the radionuclides introduced into the ocean will eventually end up in the sediments. Sev- eral aspects of nonbiological processes resulting in element— and by inference, radionuclide—recycling from bottom sedi- ments to water column are discussed in Chapter 6; that there are purely biological vectors cannot be doubted, but we know little of them. Both predation by deep-water nekton on benthic organisms and redistribution as floating eggs or planktonic larvae of benthic organisms might well prove to be significant processes. ORGANISM INTERRELATIONSHIPS IN MARINE ECOSYSTEMS The marine environment is a continuum in a sense not ap- proached by either the land or fresh waters. In addition to the significantly freer movement available to individuals or species that float or swim, the environment ensures that, subject only to their physicochemical stability, the exome- tabolites of all marine organisms are available to all the others. It is therefore not surprising that, as Connell and Orias (1964) concluded, interaction with other species should appear to be an extremely important factor in the determination of marine ecological niches. Below, we dis- cuss the possibility that this excessive closeness of species in marine ecosystems may render such systems unusually sensi- tive to radiation; it seems worthwhile also to consider whether there may be aspects of the mechanisms of species interaction that affect the radiation exposure of the indi- vidual organisms. The interaction mechanisms that appear relevant in this connection may be classified as follows: 1. Species interactions not mediated by food a. Interactions mediated by exometabolites i. Exometabolites as attractants, repellents, or anti- biotics ii. Exometabolites as complex-formers, competing for inorganic nutrients b. Interactions not mediated by exometabolites i. Indirect stimulation of growth of other species, by increase in rate of regeneration of nutrients ii. Indirect effect on the growth of other species, by altering the physical environment 2. Species interactions along food chains Interactions Not Mediated by Food Among those interactions not mediated by food, the actions of exometabolites of marine organisms as attractants, repel- lents, or antibiotics, while of considerable general interest, appear to be essentially neutral with respect to the radionu- clide metabolism of organisms. Only specific attractants that are either ingested or adsorbed and are characterized by ra- dionuclide constituents could become significant contribu- tors to the radiation exposure of the attracted organisms. No such examples have been described.

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