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CHAPTER 7 ECOLOGICAL FACTORS INVOLVED IN THE UPTAKE, ACCUMULATION, AND LOSS OF RADIONUCLIDES BY AQUATIC ORGANISMS1 Louis A. KRUMHOLZ, Department of Biology, University of Louisville, Louisville, Kentucky EDWARD D. GOLDBERG, Scripps Institution of Oceanography, University of California, La Jolla, California HOWARD BOROUGHS, Hawaii Marine Laboratory, University of Hawaii, Honolulu, T. H. Introduction THIS paper is concerned with the uptake, ac- cumulation, and loss by living organisms, of radioactive materials that may be added to or induced in an aquatic environment. These aquatic organisms may live in either fresh, salt, or brackish water and include vascular plants, algae, protozoans, plankton, all the other in- vertebrate forms such as aquatic insects, bottom- living crustaceans and molluscs, and representa- tives of each of the five classes of vertebrate animals. The accumulation and loss of any radioiso- tope will depend not only upon its own physical half-life but also upon the biological factors that contribute to its incorporation in, reten- tion by, and disappearance from the organism involved. In general, all isotopes of any one chemical element are similar in chemical behav- ior, and thus it can be assumed, when tracing the paths of most chemical elements through biological systems, that a radioactive atom will behave in the same way as a non-radioactive atom of the same species. However, relatively little is known about the actual mechanisms of uptake, accumulation, and loss by marine and fresh-water organisms of the elements whose isotopes constitute fission products and other radiomaterials. For the purposes of this discussion, the fol- lowing terms will be defined: Uptake is the amount of material that enters the organism in question and the speed at which the material enters is the rate of uptake. 1 Contribution No. 9 (New Series) from the De- partment of Biology, University of Louisville. Con- tribution from the Scripps Institution of Oceanography, New Series, No. 901a. Contribution from the Hawaii Marine Laboratory, No. 94. Loss is the amount of material that leaves the organism, and the speed at which it leaves is the rate of loss. Accumulation is the amount of material that is present in the organism at a given time, and the rate of accumulation is the amount accumulated per unit time. In practice, the accumulation is the difference between the uptake and the loss. Metabolic processes include all the chemical changes concerned in the building up and de- struction of living protoplasm. During these changes, energy is provided for the vital proc- esses and for the assimilation of new materials. Specific activity is the ratio between the amount of radioactive isotope present and the total amount of all other isotopes of that same ele- ment, both radioactive and stable. Most com- monly, it is given as the microcuries of radio- isotope per gram of total element. Although the higher animal forms are de- pendent upon the primary concentrators, the plants, for their source of energy, these animals may or may not be dependent upon the lower forms for many elements. Some elements may . enter the bodies of the higher forms directly from the water, while others must be supplied from the lower trophic levels through the food web. These food webs are not the same for all organisms and may even be different for the same organism at various seasons of the year. In some instances certain elements, although present in the environment, are not in the proper physical and/or chemical state to be util- ized by the organisms and thus are not available for metabolism. Radionuclides may become associated with an organism either through adsorption to surface areas, through engulfment, or through metabolic 69

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70 Atomic 'Radiation and Oceanography and Fisheries processes; in some instances assimilation may take place following the engulfment of living or inert participate matter. A radionuclide may also be incorporated into an organism by simple exchange of the radioactive isotope for the sta- ble isotope of the same species. It is therefore important to know the physical and chemical state necessary for metabolism, the mode of entry, and the ability of all organisms at each of the different trophic levels to concentrate the various radionuclides. Physical and Chemical Factors Concerned with the Uptake of Radionudides by Living Organisms a. Acute versus chronic exposure Chronic exposure of an aquatic organism, even to low concentrations of radiomaterials, usually has a markedly different effect on the organism than an acute exposure; the principal difference lies in the amount of radiomaterial accumulated in the tissues. Because many aquatic organisms have the ability to concentrate radiomaterials from their environments by fac- tors up to several hundred thousand, much ra- diomaterial may be accumulated during a chronic exposure for a relatively long period of time. A state of equilibrium is ultimately reached at which there is a constant uptake and a constant loss with a resultant constant maxi- mum level of accumulation. Conversely, in an acute exposure, such as a single feeding or a single injection of radiomaterials, only a certain relatively small fraction of the radiomaterial is accumulated in the body and the remainder is lost. In such an instance, the maximum level to which an organism is capable of accumulating the radiomaterial in question is seldom reached and certainly not maintained. Krumholz and Rust (1954) reported an ac- cumulation of one microcurie of strontium 90 per gram of bone in the entire skeleton of a muskrat (Ondatra zibethica) which had been utilizing foods of its own choice in the area contiguous to the Oak Ridge National Labora- tory. Certainly this instance can be presumed to represent a chronic exposure inasmuch as the animal was at least two years old and had probably lived in the area during her entire life- time. Aquatic organisms in the Columbia River below the Hanford Works and those in White Oak Creek, Tennessee, below the Oak Ridge National Laboratory, have all suffered chronic exposures to radiomaterials and have accumu- lated considerable amounts of those materials in their tissues. Hiatt, Boroughs, Townsley, and Kau (1955) found that the daily feeding of strontium 89 to the fish Ttlapia for short pe- riods of time (four days) did not increase the level of strontium retention after an apparent steady-state condition had been reached. How- ever, there are no published reports of the re- sults of long-term, controlled experiments of chronic exposures of aquatic organisms to radio- materials. The literature contains many reports con- cerned with acute exposures of aquatic organ- isms to radiomaterials. Martin and Goldberg (unpublished data), who gave single feedings of strontium 90 to Pacific mackerel (Pneumato- phorus japonicus die go), found that less than five per cent of the amount fed was retained in the body after 48 hours. Much of the five per cent that was incorporated in the skeleton re- mained there for the duration of the experiment (235 days). Boroughs et al. (1956) reported that between only one and two per cent of the strontium 89 fed to ten yellownn tuna (Neo- thunnus macro pterus) remained in the body after 24 hours. The small amount retained in the body was largely incorporated into the skele- tal structures. However, other fish (Ttlapia) which had been fed similarly prepared stron- tium 89 capsules retained about 20 per cent of the ingested material after 24 hours. After four days, the amount retained finally levelled off at values that ranged from 1.5 to 19.5 per cent of the amount ingested; the average amount re- tained was about 7.5 per cent. Here, again, the retained materials were incorporated mainly in the skeletal structures and integument. b. Chemical and physical states of the ele- ments in the environment. The chemical composition of the marine en- vironment cannot be rigorously defined. The concentrations of elements depend upon the type and location of the water mass. Although more than 90 per cent of marine waters occur at depths greater than 1000 meters, the majority of chemical analyses have been made for shal- lower waters. Because of the biological ac- tivity of the oceans and the movements and origins of water masses, the abundance of cer- tain elements appears to vary by factors greater than two orders of magnitude. However, as a

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Chapter 7 71 Ecology of Uptake by Aquatic Organisms first approximation, the chemical constituents may be considered to be much the same in all places. Fairly good approximations of the con- centrations of elements in sea water are listed in Table 1 as the numbers of atoms per million atoms of chlorine. The reported values of con- centrations of elements on which Table 1 is based frequently fail to distinguish between the solid and dissolved phases. Whereas the oceans may be considered very roughly as a homogeneous mass, most bodies of fresh water must be examined on an individual basis because of the tremendous range in their physical and chemical characteristics. Many of the elements that occur normally in the oceans are in concentrations too small to be detected by present methods or are present in only trace amounts in fresh water. The pH of fresh waters ranges from perhaps as low as 2.2 to a high of about 10.5 although the pH of most lakes and streams falls somewhere between 6.5 and 8.5. The total dissolved solids in fresh waters ranges TABLE 1 CHEMICAL ABUNDANCES IN THE MARINE HYDROSPHERE mg/1 H 108,000 He Li Be B C N 0.000005 0.2 28 0.5 O 857,000 F 1.3 Ne 0.0003 Na 10,500 Mg 1,300 Al 0.01 Si 3 P 0.07 S 900 Cl 19,000 A K . Ca Sc Ti V . Cr Mn Fe Co Ni Cu Zn Ga Ge As Se Br Kr Rb Sr Y . Zr Nb Mo Tc Ru Rh Pd 0.6 380 400 0.00004 0.001 0.002 0.00005 0.002 0.01 0.0005 0.0005 0.003 0.01 0.0005 < 0.0001 0.003 0.004 65 0.0003 0.12 8 0.0003 0.01 atoms/10* atoms Cl 202,000,000 .002 50 830 4,300 70 100,000,000 130 0.03 850,000 100,000 0.7 200 4 52,000 1,000,000 28.5 18,000 19,000 0.002 0.04 0.08 0.002 0.07 0.3 0.02 0.02 0.09 0.3 0.01 < 0.003 0.07 0.1 1,500 0.007 2.2 160 0.006 0.2 mg/1 Ag 0.0003 Cd 0.000055 In < 0.02 Sn 0.003 Sb < 0.0005 Te I 0.05 Xe 0.0001 Cs 0.0005 Ba 0.0062 La 0.0003 Ce 0.0004 Pr Nd Pm Sm Eu Gd Tb Dy Ho Er Tm Yb Lu Hg Ta W 0.0001 Re Os Ir Pt , Au .... 0.000004 Hg 0.00003 Tl < 0.00001 Pb 0.003 Bi 0.0002 Po At Rn .... 9.0 X 10-™ Fr Ra 3.0 X 10-* Ac Th 0.0007 Pa 0.003 U atoms/10* atoms Cl 0.005 0.0009 <0.3 0.05 < 0.008 0.7 0.001 0.005 0.008 0.004 0.005 0.001 0.00004 0.0003 < 0.00009 0.03 0.002 8.0 X 10-" 2.0 X 10'1* 0.006 0.03

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72 Atomic Radiation and Oceanography and Fisheries from very low concentration (less than 5 ppm) in the "battery-water" lakes to very high concen- trations (more than 400 ppm) in the "alkali" lakes. The fertility of fresh waters ranges from the almost sterile bog lakes to the highly pro- ductive lakes in the midwestern prairies. The physical states and ionic speciation of elements in sea water cannot be as well denned as their absolute concentrations. However, us- ing the known physicochemical constants, and assuming a pH of 8 and a salinity of 35 parts per thousand for sea water, Krauskopf (1956) postulated that the principal valence states of the ions of a number of metals in sea water are as listed in Table 2. From these data it may TABLE 2 CALCULATED VALENCE STATES FOR METALLIC IONS IN SEA WATER (From Krauskopf, 1956) Element Ion Zinc Zn++, ZnCl+ Copper Cu++, CuCl+ Bismuth BiO+ Cadmium CdCl+, CdCli Nickel Ni++, NiCl+ Cobalt Co+4- Mercury HgCh- Silver AgClT Gold AuClT (Calculated by Goldberg) Chromium CrOr Vanadium H.VCV, H.V,Cy Magnesium Mg++ Calcium Ca+ + Strontium Sr-f+ Barium Ba-j—\- be concluded that most monovalent or divalent ions, except the noble metals, will occur as ca- tions whereas most metals with valences higher than two, and the noble metals, will occur as anions. The physical states of a given element under equilibrium conditions depend upon whether or not the solubility product of the least soluble species has been exceeded. Greendale and Bal- lou (1954) have determined the distribution of elements among the soluble, colloidal, and par- ticulate states by simulating the conditions of an underwater detonation of an atomic bomb. Their data are presented in Table 3. It is not known whether the elements that occur in colloidal or particulate phases are homogeneous entities or are sorbed in other solid phases. Nevertheless, it appears that ele- ments of Groups, I, II, V, VI, and VII usually occur as ionic forms in sea water, whereas other elements, excluding the rare gases, occur pre- dominantly as solid phases. These generaliza- tions have been confirmed in field tests after underwater detonations where more than 50 per cent of the resultant radioactivity was associated with solid phases retained by a molecular filter of pore size 0.5 micron (Goldberg, unpublished data). Although the data supplied by Greendale and Ballou (1954) are of value for the physical states of elements following the detonation of an atomic bomb, they are at best only suggestive of the steady-state conditions which might re- sult from the continuous spilling of fission product wastes into the sea on a long-term basis. TABLE 3 PHYSICAL STATES OF ELEMENTS IN SEA WATER • (From Greendale and Ballou, 1954) Percentage in given physical state Element Cesium Ionic Colliodal Particulate 23 70 7 90 8 2 87 3 10 73 13 12 45 43 12 Molybdenum . . 30 10 60 Ruthenium .... 0 3 95 2 4 94 1 3 96 Yttrium 0 4 96 Niobium . 0 0 100 Metabolic processes concerned with the uptake, accumulation, and loss of radionuclides There are many factors concerned with met- abolic processes which are to be considered among the biological aspects of the accumula- tion of radiomaterials. It has been demonstrated that the metabolism of all forms of life is re- markably similar at the cellular level even though the morphological differences among aquatic organisms range from the bacteria through the vertebrate forms, and from the algae through the vascular plants. Nevertheless, differences do exist. These differences are gov- erned by the complex anatomies, life histories, and physiological processes, and the relation- ships of the organisms with each other and with their environment. All of these differences must be considered in the light of the physical and chemical states of the elements involved.

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Chapter 7 73 Ecology of Uptake by Aquatic Organisms In different organisms, ionized or paniculate fission-product wastes and other radiomaterials may be either adsorbed, engulfed, or accumu- lated by metabolic processes. For example, Rothstein and his associates (1951) demon- strated that uranium as the uranyl ion was ad- sorbed by yeast cells. Hamilton and co-workers (see Hevesy, G., 1948, p. 441) showed that particulate radiomaterials such as various un- complexed rare earths at physiological pH's were adsorbed by the gut lining of rats. In these experiments practically no accumulation of these particular radiomaterials by the animal was observed. On the other hand, Goldberg (1952) demonstrated with radioactive iron that a marine diatom assimilated particles of hy- drated iron oxide, but that these organisms were unable to take up ionic iron in a complexed form. The first biological experiments in which ra- dioactive atoms were used were performed by Hevesy in 1923. In those classical experiments it was demonstrated that plants could take up lead from solution and translocate it throughout the vascular system. The accumulation of radioelements is also de- pendent upon many chemical characteristics of the water in question. Among the parameters affecting accumulation are the salinity, percent- age composition of the dissolved solids, pH, the oxygen-carbon dioxide ratio, and the presence of complexing agents. a. Chemical composition of marine organisms A modern systematic study of the inorganic constituents of marine organisms is yet to be made. The best summary of existing knowledge may be found in Vinogradov (1953). However, certain generalizations can be drawn from the recent literature on the concen- tration of metals by marine organisms. Gold- berg (in Treatise of Marine Ecology, volume II, edited by J. Hedgpeth, in press) has pointed out that the marine biosphere tends to concen- trate such heavy metals as copper, nickel, zinc, etc., over the marine hydrosphere by factors of 100 to 100,000 on a weight-for-weight basis (Table 4). These metals are strongly bound in the organisms and cannot be easily removed by elution. Further, the elements most strongly concentrated in the biosphere are those that form the most stable complexes with organic chelating agents. As an example, copper is con- centrated over sea water in the soft parts of most marine organisms by factors of 102 to 10* whereas calcium shows concentration factors of less than 1 to 50. Copper forms very strong complexes with many organic compounds whereas calcium does not. Although the exact role of most metals in the physiology of organ- isms is not known, nevertheless, one might a priori expect that some heavy metals introduced into the ocean from nuclear reactions would concentrate in the biosphere. b. Concentration in the environment The concentration of a given radiomaterial by an organism is sometimes proportional to the concentration of that material in the en- vironment. This generalization applies both to aquatic and to terrestrial organisms. The uptake of cesium 137 by the oyster (Crassostrea vir- ginica) has been shown to be dependent upon the external concentration of cesium in the sea water (Chipman, et al., 1954). Prosser, et al. (1945), noted that with the addition of stron- tium to the environment there was an increase in the uptake of that element by goldfish (Coras- sius auratus). Also, it has been demonstrated that as the carrier concentration in the nutrient environment is increased, the concentration fac- tor for a particular fission product in terrestrial plants tends to increase (Rediske, et al., 1955). c. Effect of the presence of one element on the uptake of another element The uptake of one radioelement by an organ- ism may be altered by the relative abundance of another element in the environment. In instances in which more than one element is involved, one of three phenomena may be observed: First, elements of similar chemical properties may substitute for one another. For example, it has been shown by Prosser, et al. (1945), that when the amount of calcium in the water was low, there was an increase in the uptake of strontium 89 by goldfish. Conversely, as the amount of calcium was increased, the uptake of strontium decreased. Rice (1956) observed that cells of Carteria grown in artificial sea water took up strontium in proportion to the stron- tium/calcium ratio in the medium. Bevelander and Benzer (1948) have shown that a modifica- tion of the constituents of sea water resulted in a change in the constituents of the shells de- posited by mollusks. Second, some elements may have an inhibi- tory effect on others. A classical example of this

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74 Atomic Radiation and Oceanography and Fisheries phenomenon is that in which calcium inhibits the stimulatory action of potassium on heart muscle. Third, there may be a synergistic effect of one element on another. Ketchum (1939) has shown that the uptake of phosphorus by marine diatoms was enhanced with increased concen- trations of nitrogen. d. Specificity of organisms and tissues for given elements The specific activity of a radionuclide in any present in the flight muscles of some birds and it has been shown that radiophosphorus is in- corporated into the flight muscles of migratory waterfowl (Krumholz, 1954). Although many different kinds of aquatic or- ganisms have the ability to concentrate phos- phorus in their tissues, there are few that show such a specificity for that element as the various plankters. The uptake of phosphorus 32 by plankton algae in a lake has been demonstrated by Coffin and his associates (1949) and others, TABLE 4 APPROXIMATE CONCENTRATION FACTORS OF DIFFERENT ELEMENTS IN MEMBERS OF THE MARINE BIOSPHERE. THE CONCENTRATION FACTORS ARE BASED ON A LIVE WEIGHT BASIS. Concentration Factors c loncentration in seawater iicrograms/1.) 10' 380,000 0.5 400,000 7,000 10 3 10 2 10 1 1 0.05 70 900,000 50 Algae (Non -cal- careous) 1 25 1 10 20 100 100 20,000 500 10 1,000 1,000 300 10,000 10 10.000 Invertebrates Vertebrates Element Na ... Form in Seawater (rr Ionic Soft 0.5 10 10 Skeletal 0 0 Soft Skeletal 0.07 1 5 20 10 — 1 200 1 200 1,000 30,000 1,000 1,000 1,000 5,000 100 — 20 — 20 — 40 — K Ionic Cs Ionic Ca , . . . . Ionic 10 1,000 1,000 1,000 5,000 100,000 200 Sr , . . . . Ionic 10 5,000 5,000 10,000 200 100 100 1,000 Zn Ionic Cu . . .... Ionic Fe Particulate Ni ! Ionic Mo .... lonic-Particulate V Ti j Cr j P Ionic 10,000 5 100 10,000 40,000 2,000,000 2 — 10 — s 1 50 I . 1 Values from Laevastu and Thompson (1956). organism is dependent upon the ability of the organism or any of its parts to concentrate that nuclide. If the stable counterpart of the radio- nuclide does not normally enter into the physio- logical processes of an organism, neither will the radioactive material. It is well known that certain tissues have a predilection for concentrating specific elements. For instance, iodine is concentrated in the thy- roid tissue of animals and hence radio-iodine will also be concentrated there. Strontium, like calcium, is a bone seeker and the radioisotopes of both of those elements will be concentrated in the bony skeletons of animals. Similarly, both strontium and calcium are concentrated in certain parts of vascular plants and so are the radioisotopes. Phosphorus is one of the princi- pal constituents of bone and radiophosphorus is also concentrated in that tissue. The com- pound adenosine triphosphate is commonly and Whittaker (1953) showed that phyto- plankters from the Columbia River concentrated radiophosphorus by factors as great as 300,000. Krumholz (1954, 1956) found that attached fresh-water algae (Spirogyra) concentrated ra- diophosphorus by a factor of 850,000, and that many fresh-water zooplankters concentrated that radionuclide by factors of more than 100,000. Approximate concentration factors for marine organisms are given in Table 4. e. Osmotic and ionic regulation Osmotic and ionic regulation are known to occur in a variety of ways. The usual pathways of excretion are through the urine, feces, skin, respiration, and particle ejection, and the method of excretion depends upon the particu- lar organism and element involved. Ionic regu- lation may also occur by way of the chloride secreting cells in the gills of those fishes that migrate from salt to brackish water (Keys,

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Chapter 7 73 Ecology of Uptake by Aquatic Organisms 1931). Unfortunately, no experiments on such ionic regulation have been performed with ra- dionuclides. f. Reproductive processes The reproductive processes of plants and ani- mals range from simple fission among the unicellular organisms to the very complex rela- tionships among the gametogenic forms. Dur- ing reproduction there is a transfer of materials from the parent to the offspring. In simple fission, the parent cell splits in two and each offspring receives approximately half of the parent material and thus only half of any radiomaterial that may have been pres- ent. Under conditions of chronic exposure, the offspring of organisms that reproduce by fission will incorporate usable radiomaterials into their bodies and a state of equilibrium eventually will be reached. Among the egg-laying forms, most of the material received by the offspring is derived from the contents of the egg. In this form of reproduction, once the egg is laid there will be no further loss of radiomaterials from the mother or gain to the offspring. This applies even when the environment is contaminated and there is chronic exposure of the parents, because the protective coverings of the egg pre- vent the entrance of radiomaterials. Among the forms that bear their young alive, however, there is usually some continuous trans- port of materials between the mother and the embryo. In such an instance it is probable that the embryo will accumulate radiomaterials with a resultant loss to the mother. If chronic ex- posure of a mother carrying an embryo con- tinues during pregnancy, a state of equilibrium may eventually be reached between the mother and the environment and between the mother and the embryo. During embryological development of all kinds there is a "biological dilution" of radio- materials through cell division and growth. This statement applies primarily if there has been an acute exposure to radiomaterials or if the ex- posure has stopped with the commencement of the embryological development. g. Molting In instances where the embryos pass through a series of metamorphic stages, there is a loss of radiomaterials from stage to stage as, for ex- ample, the loss from instar to instar in insects through molting. Furthermore, it has been demonstrated by Chipman and coworkers (per- sonal communication) that there is an increased accumulation of elemental constituents in crus- taceans prior to molting, and a loss of such ma- terials when the carapace is lost. h. Age and growth It has been established (Olson and Foster, 1952) that younger, more rapidly growing fishes accumulate relatively greater amounts of radiomaterials than do older, more slowly grow- ing individuals. This phenomenon is probably a reflection of the more rapid metabolism that accompanies the growth of the younger fishes. It is not known whether the accumulation of radiomaterials by other aquatic vertebrates and invertebrates is a function of age and growth. i. Effect of temperature on cold-blooded and warm-blooded animals In general, the body temperatures of warm- blooded animals are more or less constant whereas the body temperatures of cold-blooded animals largely depend upon the temperature of the environment. Similarly, the rate of metab- olism in warm-blooded animals is generally in- dependent of temperature changes in the en- vironment while that in the cold-blooded animals is largely dependent upon external temperatures. Changes in temperature affect the rates of chemical reactions and hence chemi- cal processes that involve the accumulation of elements in the body tissues are temperature dependent. Generally speaking, all cold-blooded aquatic organisms exhibit seasonal changes in the up- take and accumulation of radiomaterials from the environment. Davis, et al. (1953), and Krumholz (1954, 1956) have shown that there is a direct correlation between an increase in temperature and an increase in the accumulation of radiomaterials in fishes of the Columbia River, Washington, and of White Oak Lake, Tennessee, respectively. This increase in accumu- lation is apparently a reflection of the increase in the speed of the metabolic processes with rising water temperatures. However, Krumholz (1956) suggested that the fishes in White Oak Lake entered a period of dormancy following August 1 and lost about two-thirds of their ac- cumulated radioactivity during the subsequent two months even though the water tempera- tures were much the same as they were during the earlier part of the summer. In studies of the uptake of strontium 89 by

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76 Atomic Radiation and Oceanography and Fisheries oysters and other shellfish at the Radiation Laboratory of the Fish and Wildlife Service (Chipman, unpublished data) it was found that the rate of uptake was slowed down and the re- tention time was extended when the animals were kept in sea water at low winter tempera- tures. Conversely, the rate of uptake was speeded up and the retention time was short- ened when the animals were kept at summer temperatures. In other experiments at the same laboratory, it was found that larvae of the win- ter flounder (Pseudopleuronectes americanus) took up strontium 89 much more rapidly at higher water temperatures than at lower. So far as is known, there is no demonstrable seasonal pattern of accumulation of radioma- terials among the warm-blooded aquatic verte- brates. It is generally believed that inasmuch as the body temperatures of those animals remain more or less constant throughout the year there will be no marked seasonal changes in the up- take of radiomaterials based on changes in rates of metabolism. j. Effect of light Light affects the uptake and accumulation of radioelements by plants. For example, it has been clearly shown by Scott (1954) that the up- take of radiocesium by the algae Fucus and Rhodymenia was greatly enhanced in the pres- ence of light. k. Radiation effects Many aquatic organisms have the ability to concentrate radiomaterials in amounts deleteri- ous to their well-being. These deleterious effects range from those in which only the individual is concerned to those in which the population as a whole may be affected. Elsewhere in this series of reports there is a paper on the effects of radiation on aquatic organisms. Aspects of the accumulation of radionuclides through the ecosystem For purposes of this paper, the aquatic bio- sphere can be divided into three trophic levels based on energy sources: 1. Primary producers, such as the photosyn- thetic plants. 2. Primary consumers, the herbivores, such as water fleas (cladocerans). 3. Secondary consumers, the carnivores, such as the largemouth bass or the tunas. The community biomass (the total weight of all organisms in the community) is unequally divided between the three trophic levels. Usu- ally there is a progressive decrease in both the biomass and the number of organisms from the first trophic level through the third, and a pro- gressive increase in the size of the organisms. However, most community populations are con- stantly changing and are affected by seasonal, diurnal, and other cycles of abundance. These changes frequently have a profound effect on the environment and any changes in the en- vironment in turn affect the stability of the community. Generally speaking, the smaller organisms have a higher reproductive potential, a shorter life span, and a shorter time between genera- tions; the length of the life span and the time between generations usually give a fair indica- tion of the length of the embryological period. Furthermore, the smaller animals usually serve as food for the larger ones. The discussion will consider the following aspects of the accumulation of radiomaterials in the three trophic levels: (1) the distribution of elements among the three levels, (2) the concentration factors in different organisms within the same level, and (3) the transport of radiomaterials from one trophic level to another. Problems of the distribution of radionuclides among the trophic levels and the degree of con- centration of radionuclides by different organ- isms can be approached most readily through separate consideration of the effects from an acute exposure and those from a chronic ex- posure. A steady-state condition will be approximated when the amounts of radiomaterials introduced into the environment is equal to the amount that disappears through physical decay. Any organisms living in such an environment will suffer chronic exposure to the radioactivity, the level depending, of course, on their ability to concentrate the radiomaterials introduced and on the steady-state concentration of these ma- terials in the surrounding medium. An approxi- mation of the concentration factors for some organisms is given in Table 4. Davis and co-workers (1952) showed that there was a progressive decrease in the amount of radioactivity found in the aquatic organisms of the Columbia River downstream from the Hanford Works. There, the principal radionu-

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Chapter 7 77 Ecology of Uptake by Aquatic Organisms elide was phosphorus 32, which has a physical half-life of about 14 days. It is apparent that when following the steady-state transport of radiomaterials through the ecosystem the follow- ing parameters must be considered: (1) the physical half-life of the radionuclide, (2) the distance of the organism from the source of radioactive contamination, and (3) the dilution of the radiomaterials between the point of in- troduction and the area in which the organism lives. The results from acute exposure cannot be as definitely approximated as for chronic exposure. In such instances, the time element is very im- portant, and the following must be known: (1) the rate of dilution of the radioactive water mass with non-radioactive water; (2) the rate of transfer of radiomaterials from one trophic level to another with the concurrent dilutions and losses or gains in concentration by the or- ganisms; and (3) the life span of the organ- isms involved. In general, the radiomaterials taken up by organisms of the first trophic level will be pri- marily in the ionized state although a certain amount of particulate radiomaterials will be ad- sorbed to the body surfaces. When uptake oc- curs, the rate of uptake will probably be more rapid than the rate of uptake in the other trophic levels. Particulate radiomaterials tend to be concen- trated in the second trophic level. Findings from the Wigwam and Castle tests (Goldberg, unpublished data) showed that the principal or- ganisms which concentrated particulate radio- materials were the mucous, ciliary, and pseudo- podial feeders among the zooplankters. These organisms contained much more radioactivity per unit weight than either the algae or the setal or rapacious feeders. In addition to the differences in concentration of radiomaterials from one trophic level to an- other, there are marked differences among spe- cies in the same level. For instance, it has been shown by Chipman, et al. (1953), that some phytoplankters will concentrate radiostrontium by a factor of about 20 times whereas others will concentrate the radioelement by factors as much as 1500 times. Comparable data have been recorded by Krumholz (1954) for the accumu- lation of radiophosphorus by the phytoplankters of White Oak Lake. Differences also exist between individuals of the same species. Very large differences in the amounts of radiomaterials accumulated by indi- vidual fishes in White Oak Lake were described by Krumholz (1956). For instance, he reported that the amounts of radiostrontium in the bones of three bluegills (Lepomis macrochirus) dif- fered by more than five-fold. These three fish were taken from the same place in the lake on the same day, August 27, 1952. Comparable differences were found in the amounts of ac- cumulated radiomaterials in most other tissues. The transfer of radiomaterials from one trophic level to another is not only dependent upon the concentration of the radiomaterial in the organism but also is governed by the rate of growth of the organism and the rate of in- crease in the size of the population. These fac- tors of transfer are of particular importance in the event of an acute exposure because the dilu- tion brought about through cell division and growth may well minimize any radiation effect. In any event, there is always a loss in the total amount of radiomaterials in the transfer from one trophic level to another (though not nec- essarily a decrease in the concentration in indi- vidual organisms). Such a loss may be rela- tively small or it may be very great depending upon the organism and the particular food web involved. Not all radiomaterials that enter the first trophic level are passed on to higher levels. At each trophic level there are certain species that, for one reason or another, are not widely used as food by the organisms of higher levels. Also, some of the plants of the first trophic level may die before they are eaten and thus will be re- turned to the environment as organic matter. In this case the primary producers may be of little or no importance as a source of radioma- terials to the organisms of the second and third trophic levels. If relatively large quantities of radiomaterials are accumulated in certain hard parts of an or- ganism, such as the shell of an oyster or the bones of a fish, they will, in all probability, re- main in those parts during the greater part of the life of the animal concerned, and will not be available to other animals in the biosphere until the animal dies. Chipman and co-workers (1953) showed that oysters fed on Chlorella assimilated only very little of the radiophosphorus from these

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78 Atomic Radiation and Oceanography and Fisheries algae. On the other hand, oysters fed upon other phytoplankters that contained no more ra- diophosphorus than the Chlorella accumulated relatively large amounts of radiophosphorus and incorporated that element into their tissues as organic phosphorus compounds. It appears that the particular food web used by any organism is of primary importance in the transfer of ra- diomaterials from one trophic level to another. Problems for further research One of the fundamental questions to be an- swered concerns the mechanism of incorpora- tion of the heavier elements, such as the fission products, in aquatic organisms. To date, no metal heavier than molybdenum has been shown to be necessary for metabolic processes. Spe- cifically, we need to know: 1. How are the radioactive elements passed through membranes and where and why do they concentrate in the organisms ? 2. What are their biological half-lives of the different radioactive elements in different or- ganisms ? 3. What are the average and extreme concen- tration levels of these elements in various or- ganisms and in the biosphere? The revolution in biological thought brought about by the use of labelled atoms is manifest in all branches of biological research today. Radioisotopes have permitted the study of rate processes that could not have been investigated in any other way. Such processes include the pumping rates of water and other biological fluids, and the transfer of molecules or portions of molecules from tissue to tissue, or, on the ecological level, from organism to organism. REFERENCES BEVELANDER, G., and P. BENZER. 1948. Cal- cification in marine molluscs. Biol. Bull. 94:176-83. BOROUGHS, H., S. J. TOWNSLEY and R. W. HIATT. 1956. The metabolism of radio- nuclides by marine organisms. I. The uptake, accumulation and loss of strontium 89 by fishes. Biol. Bull. 111:336-351. CHIPMAN, W. A., T. R. RICE, and T. J. PRICE. 1953. Accumulation of radioactivity by marine invertebrate animals. U. S. Fish and Wildlife Service Radioisotope Labora- tory, Progress Report, April 1953, (Type- written) . 1954. Accumulation of fission products by marine plankton, fish, and shellfish. U. S. Fish and Wildlife Radioisotope Labora- tory, Progress Report, July-December 1954, (Typewritten). COFFIN, C. C, F. R. HAYES, L. H. JODREY, and S. G. WHITEWAY. 1949. Exchange of ma- terials in a lake as studied by the addition of radioactive phosphorus. Canad. Jour. Research 27:207-222. DAVIS, J. J., R. W. COOPEY, D. G. WATSON, C. C. PALMITER, and C. L. COOPER. 1952. The radioactivity and ecology of aquatic organisms of the Columbia River. In Bi- ology Research — Annual Report, 1951, USAEC Document HW-25021, pp. 19-29. GOLDBERG, E. D. 1952. Iron assimilation by marine diatoms. Biol. Bull. 102, 243-8. GREENDALE, A. E., and N. E. BALLOU. 1954. Physical state of fission product elements following their vaporization in distilled water and seawater. USNRDL Document 436, pp. 1-28. HEVESY, G. 1923. Absorption and translocation of lead by plants. Biochem. Jour. 17:439- 45. 1948. Radioactive indicators. Interscience Publishers, New York, xvi + 555 pages. HIATT, R. W., H. BOROUGHS, S. J. TOWNSLEY, and GERALDINE KAU. 1955. Radioisotope uptake in marine organisms with special reference to the passage of such isotopes as are liberated from atomic weapons through food chains leading to organisms utilized as food by man. Hawaii Marine Laboratory, Annual Report, AEC project number AT(04-3) 56, pp. 1-29, (Mimeo- graphed) . KETCHUM, B. H. 1939. The adsorption of phosphate and nitrate by illuminated cul- tures of Nitzckia closterium, Am. J. Botany 26:399-402. KEYS, A. B. 1931. Chloride and water secre- tion and absorption by gills of die eel. Zeitsch. Vergl. Physiol. 15:364.

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Chapter 7 79 Ecology of Uptake by Aquatic Organisms KRAUSKOPF, K. B. 1956. Factors controlling the concentrations of thirteen rare metals in sea water. Geochim. et Cosmochim. Acta 9:1-32. KRUMHOLZ, L. A. 1954. A summary of find- ings of the ecological survey of White Oak Creek, Roane County, Tennessee, 1950- 1953. USAEC Document ORO-132, pp. 1- 54, (Mimeographed). 1956. Observations on the fish population of a lake contaminated by radioactive wastes. Bull. Amer. Mas. Nat. Hist. 110(4) :277- 368. KRUMHOLZ, L. A., and J. H. RUST. 1954. Osteogenic sarcoma in a muskrat from an area of high environmental radiostrontium. A.M.A. Arch. Path. 57:270-278. LAEVASTU, T., and T. G. THOMPSON. 1956. The determination and occurrence of nickel in sea water, marine organisms and sedi- ments. /. duCons. 21:125-143. OLSON, P. A., JR., and R. F. FOSTER. 1952. Effect of pile effluent water on fish. In Biology Research — Annual Report, 1951. USAEC Document HW-25021, p. 41. PROSSER, C. L., W. PERVINSEK, JANE ARNOLD, G. SVIHLA, and P. C. TOMPKINS. 1945. Accumulation and distribution of radio- active strontium, barium-lanthanum, fission mixture and sodium in goldfish. USAEC Document MDDC-496, October 13, 1954. REDISKE, J. H., J. F. CLINE, and A. A. SELDERS. 1955. The absorption of fission products by plants. In Biology Research — Annual Report, 1954. USAEC Document HW- 35917, pp. 40-46. RICE, T. R. 1956. The accumulation and ex- change of strontium by marine and plank- tonic algae. Limnology and Oceanography 1(2):123-138. ROTHSTEIN, A., and R. MEIER. 1951. The re- lationship of cell surface to metabolism VI, the chemical nature of the uranium com- plexing groups of the cell surface. /. Cell. Com p. Physiol. 38:245-70. SCOTT, R. 1954. A study of cesium accumula- tion by marine algae. Proc. Second Radio- isotope Conference, pp. 373. VINOGRADOV, A. P. 1953. The elementary composition of marine organisms. Sears Foundation for Marine Research, Memoir No. 2. WHITTAKER, R. H. 1953. Removal of radio- phosphorus contaminant from the water in an aquarium community. In Biology Research-Annual Report, 1952. USAEC Document HW-28636, pp. 14-19.