Radioactivity in the Marine Environment (1971)

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206 Radioactivity in the Marine Environment The reaction of exometabolites as complex-formers is, however, clearly of importance in controlling the balance of distribution of adsorbable radioelements between neutral surfaces and organisms. Even excreted orthophosphate may be expected to significantly resolubilize lanthanides attached to sediment surfaces, and such large molecules as the phos- phate compounds released by marine plankton algae (Bowen and Campbell, unpublished experiments) or the amino acids known from zooplankters (reviewed by Stephens, 1968) could be expected to be more effective. Such tightly linked species associations as we infer for marine ecosystems can be expected, then, to be unusually efficient in recycling ad- sorbed elements, whether physiological or not, and conse- quently to be more subject to radiation exposure from introduced nuclides. A third aspect of species interlinkage in the oceans is the provision it gives for recycling of specific plant-nutrient ele- ments. The evolutionary value, to an ecosystem, of linkage of this sort is obvious, but such recycling cannot be limited only to nutrients in demand. It was suggested by Ketchum and Bowen (1958) that in some situations and in some en- vironments the same relationships responsible for nutrient recycling should result in long-term retention of nonphysio- logical elements, or radionuclides, in the euphotic zone. Bowen and Sugjhara (1965) described a situation in which this mechanism appeared to have operated for fallout 144Ce. Again, the very aspect of the close-linked system that gave it evolutionary advantage may sometimes act to increase its exposure to radiation. Especially in near-shore areas, but also in other marine environments, an important aspect of species interlinkage is clearly the physical effect of one species in making the envi- ronment more suitable for another, whether in producing shade, in preconditioning-or providing-a settling surface, or in mechanically damping out the force of water move- ments. It is not evident, however, that the special nature of any of these interactions should increase the radiation sensi- tivity of the ecosystems in which they operate. It appears then, that of the various ways in which marine species are especially closely linked, other than as food, some may, by virtue of their special properties, increase the potential for radiation exposure of the ecosystem, while others appear to be essentially neutral. We have not dis- cerned any that appear to have contributed to decreased radiation exposures. Interactions Mediated by Food or Feeding "Perhaps the most challenging and complex problem in the ocean is the question of how organic matter is formed and how it moves through the food web of marine organisms."* 'National Academy of Sciences-National Research Council (1967, p. 52). Ecologists have found it useful in attempting to define regu- larities in this problem to erect a variety of hierarchies based on feeding relationships-food chains, food webs, or feeding cycles. In most of these hierarchies, the concept of trophic level appears, as an indication of how far removed a species is from direct feeding on the primary producers-photosyn- thesizing plants. Usually, trophic level I refers to the photo- synthesizing plants, level II to the grazers or herbivores, level III to predators on herbivores, level IV to predators on level III predators, and so on. There is general recognition of the factors that blur the distinctions between trophic levels— i.e., that few species have simple feeding habits, that for many species the food emphasis shifts during the life cycle, and that for others it may shift even seasonally. The concept is still useful and has suggested a variety of theoretical and model studies of natural populations, even though in such practice, fractional trophic levels often are required (tuna, for instance, are best viewed as occupying trophic level IIIi£, according to Schaefer, personal communication). An interesting aspect of the marine, as opposed to terres- trial, food chains is the generally small range of sizes of her- bivores; in the open ocean, this appears to be a clear conse- quence of the generally tiny size of the primary producers, but even in the kelp forests, no herbivores of sizes compa- rable to the large terrestrial mammals have appeared. It is likely that this size factor is chiefly responsible for the longer food chains of the oceans. The continuity of the physical environment, however, has another important con- sequence: Other than the efficiency factor, there is no bar to short-circuiting of their food chains by higher trophic levels. A salp or euphausiid is as accessible to a tuna as is a herring-quite unlike otherwise comparable situations on land. And, because of the size differences and consequent increase of the surface-to-volume ratio, such short-circuiting may always be assumed to lead to an increase in exposure of the higher level to adsorbable radioactivity in the environ- ment. Another possibly important result of this combination of environmental continuity and prevalent small size of prey has been the repeated evolution, by marine organisms, of feeding by means of mucous threads or sheets. It is assumed that these are "intended" principally as traps for small or- ganisms and nutritive detritus particles. We do not know whether there has been positive selection for mucous having strong ion-exchange properties and consequent good effi- ciency at trapping dissolved organic molecules, or whether this property has developed only as a by-product in the evo- lution of suitable mechanical properties of the mucous. It is clear, however, that many mucopolysaccharides, especially those with strong sulfuric acid residues, have powerful ion- exchange properties. Goldberg (1957) emphasized this phe- nomenon in both selective and nonselective bioaccumulation of elements from seawater. Since mucous feeding is usually mediated by actual ingestion of the mucous and its digestion along with the load of trapped food [often on a regular and

Ecological Interactions of Marine Radioactivity 207 rapid cycle (Prosser and Brown, 1961, p. 107)], this habit must greatly increase an organism's exposure to radionu- clides in his environment, even those that are wholly non- physiological and represented by negligible concentration factors. The generalization has been made that only about 10 per- cent transfer efficiency per food-chain step is typical for many elements, as it seems to be for energy (Slobodkin, 1968; Schaefer, 1968). When they are studied with radio- nuclide tracers, many elements have appeared subject to discrimination, or a reduction in mass concentration through each step in a trophic series (see Baptist and Lewis, 1969, for data and a review). Odum (Odum and Golley, 1963), in fact, was so impressed by the parallelism in this respect be- tween transmittal of some elements and energy along food chains that he proposed the use of radionuclides of zinc or phosphorus as "indices of energy flow" in ecosystems. It has been frequently concluded that man, in drawing little food from marine primary producers, only moderate amounts from marine grazers, and most from predators at fairly high trophic levels, places an effective barrier between himself and radioactive nuclides introduced to the oceans (National Academy of Sciences-National Research Council, 1962, p. 52). Examination of the large amount of data now avail- able shows clearly that the situation is by no means so simple; this is, in fact, an example of the "unrealistic safety factors" referred to by Revelle (1959). The use of stable-element "concentration factors"— derived from chemical analysis of both the medium and the organisms-has been frequently proposed and used to pre- dict both the places of major entry of introduced radionu- clides into food webs and the concentrations to be expected in the various organisms involved. The use of such data is basic to the "specific activity approach" (National Academy of Sciences-National Research Council, 1962), but they have proved useful in other contexts as well. Some of the reservations to be applied to their use, however, are serious, as has already been discussed in the consideration of the uses of concentration factors (Chapter 1). Briefly, we may note here two of the most salient reser- vations; they stem from our uncertainty of the time con- stants of element uptake or excretion and also from our uncertainty of the physical and chemical environment in which uptake occurs: Time Constants of Uptake or Excretion Strictly speaking, one can expect the stable-element and radionuclide concen- tration factors to be the same only when the specific activity of the radionuclide in the medium has remained about con- stant over several biological half-lives of the nuclide in the organism. This implies uniform labeling over time as well as space. It is, however, very unusual for us to know the bio- logical half-life of an element in any marine organism; as Kuenzler (1969a, b) has shown, such measurements as can be made are in most cases of questionable generality. The ideal situation must, of course, be approached as the life cycles of the organisms considered are shorter, and the least favorable situation must be approached in those large organ- isms that immobilize much of a given element metabolite, whether in massive skeletons, in stored reserves, or in stored excreta. Conversely, predictability must be favored in situ- ations where a nearly uniform flux of radionuclide is main- tained over long periods, in a relatively restricted environ- ment, as in the Columbia River outflow under constant operating levels at Hanford. The Physicochemical State of Radionuclides and Stable Element in the Environment Even in the open ocean, we have inadequate data on the physicochemical states of ele- ments or of their nuclides and on the rates of equilibration among these (see Chapter 5). As discussed by Jones (1960), among others, this ignorance has made radioruthenium re- lease behavior essentially unpredictable. Bernhard and Zattera (1969) have presented data illustrating uncertainty of the fractions of seawater zinc available as carrier for intro- duced 65Zn; data on 55Fe in Pacific salmon may be used to raise the same sorts of question (Jennings, 1968). With re- spect to benthic organisms, especially those that feed largely within the sediment, there seems to us to be complete un- certainty about what might be taken as the "environmental" concentration of any trace elements; this is a severe bar to using such data as those of Phelps et al. (1969) in a predic- tive way. Unfortunately, however, the literature dealing with the uptake of radionuclides released to environments appears just as difficult to use for prediction. Either the physico- chemical constants of the local environment are too little known to support extrapolation of data to new situations or the local time-constants for exposure levels are comparably little known, or both. This situation is well illustrated in a massive study (Seymour and Lewis, 1964) of the Columbia River effluent contaminations of marine organisms, sedi- ment, and water from 1961 through 1963. In spite of the enormous amount of data collected, often on the same spe- cies from several different locations, very little generaliza- tion was possible, largely, one feels, because of uncertainty about precise exposure times or levels and because of local variation in stable nuclide diluents. Jennings (1968) points out data (his and those of Kujala et al., 1969) that indicate that "available" levels of several elements (notably Mn, Zn, and Fe) are higher inshore than offshore, and may be sub- ject to local variation as well. In view of this, we feel the best approach to prediction of radionuclide behavior in ecosystems is still by use of stable-element analytical data, suitably qualified by exami- nation of such tracer studies as seem applicable. Accordingly, we have summarized a considerable number of analyses of marine organisms, mostly of the open ocean; species have

208 Radioactivity in the Marine Environment been chosen about which some trophic-level conclusions could be drawn. In Table 2 are set out, from the literature or from data of Bowen et al. (to be published), the ranges of concentration factors, for a variety of elements, observed in a variety of primary producers and grazers as well as predators at various trophic levels in the marine environment. These data by no means represent a complete summary of all available data, but they appear to be reasonably consistent as a body and to illustrate the complexity of biological concentration pro- cesses. It must be noted, however, that no data are now available to show the extent of seasonal variability of ele- ment composition in most marine groups. For several bivalve grazers, such variability is known to be appreciable (Hobden, 1967; Shimizu, 1967), as it is for many attached algae (Black and Mitchell, 1952); variation in some organic com- ponents of Calanus (Comita et al., 1966) shows that it is likely that plankton species also exhibit seasonal variations of inorganic composition. This is clearly an important area in which more research would be of great value. In Figure 1 we have summarized the data of Table 2 for easier visuali- zation. A direct reduction of about an order of magnitude in concentration factor at each higher trophic level is indeed seen in tracer studies of cerium, ruthenium, and zirconium, as Baptist and Lewis (1969) reported for 65Zn; Osterberg et al. (1964) reported even greater decreases from grazers to predators in respect to 95Zr-95Nb and 141Ce, but this may have represented 1.5 to 2 trophic-level steps. Of the stable elements, however, only iodine exhibits a systematic de- crease in concentration factor at each higher trophic level; the other stable trace elements exhibit great variation in be- havior. An arbitrary, but we think useful, indicator of radio- nuclide behavior in ecosystems is the occurrence of concen- tration factors as high as 104 in the range exhibited by the groups tabulated. Applying this criterion, the grazers clearly show the greatest prevalence of high concentration factors: 104 appears in the range of six elements in the planktonic and of seven in the benthic grazers, whereas it appears for only three elements in the benthic and four in the plank- tonic algae, and for five, three, and three elements in the three groups of predators tabulated. As noted above, we do not know precisely how data on benthic predators might be compared to these values. We believe that examination in detail of the data summarized in Table 2 and in other sum- maries pertinent to this question shows that this is a real property of aquatic trophic networks and that of those ele- ments that are ever strongly concentrated by organisms, the chances are that the highest concentration factors and the most frequent occurrence of high concentration will be among grazing organisms. Cs, Mo, Ce, or Ru, never strongly concentrated by organisms, are clear exceptions, but Sr, strongly concentrated only in the skeletons of Acantharia, falls within this generalization. It hardly seems necessary to emphasize that in any par- ticular situation, such a probabilistic statement may be ex- pected not to hold. The number of exceptions, already noted, shows clearly that there is no substitute for the evalu- ation in detail of each exploited food web known to have been contaminated (as advocated in Chapter 10); however, since man is continually faced with the problems of making predictions in the absence of such evaluations, we feel that such a summary of the statistics available provides a useful guide. THE POSSIBLE RADIOSENSITIVITY OF MARINE ECOSYSTEMS In earlier discussions (National Academy of Sciences- National Research Council, 1957, p. 32), it was emphasized that planktonic or pelagic marine organisms are exposed to levels of background radiation lower than those experienced by any other populations except those in freshwater lakes living at depths below 100 m but not near the bottom. That report, however, considered exposure only to cosmic rays or to beta or gamma radiation from 40K. More recently, Polikarpov (1966), Cherry (1964), Yermolayeva-Makovskaya et al. (1968), and Beasley (1969) have presented evidence that alpha-particle doses from 226Ra or 210Po contained in marine organisms may be very high and that the low back- ground levels in the marine environments, cited by the Na- tional Academy of Sciences-National Research Council (1957) may be gross underestimates. That these high alpha exposures apply generally to marine organisms is not yet well established, while the low cosmic ray and 40K back- grounds rest on much data. We are also inclined to believe that the world ocean rep- resents the oldest environment continuously available to living organisms. It must be possible, then, that in their long history of evolution, possibly under exceptionally low radi- ation levels, the organisms of the oceans have selected against those genes responsible for radiation resistance, and may consequently be consistently more radiation sensitive than are the better known species of the land. This is Polikarpov's view (1966). The very small amount of direct evidence bearing on this question is considered in Chapter 9 of this report. As ecologists especially conscious of the di- versity of species of marine organisms and of the very small number that have thus far been maintained in culture (Mullin and Brooks, 1967; Conover, 1968), we must caution against overly broad generalization from currently available data concerning the radioresistance of marine organisms.* 'In fact, Angelovic and Engel (1970) have recently summarized data showing that such common marine organisms as the grass shrimp (Palaemonetes pugio) and the mummichog (Fundulus heteroclitus)

Ecological Interactions of Marine Radioactivity 209 Such data have derived only from the "toughest" species, since only these are maintainable for experiment. Although it is by no means clear that any correspondence exists be- tween sensitivity to radiation and to laboratory manipula- tion, caution is indicated. Furthermore, many fundamental marine species-ecologically speaking—undergo periodic population minima in response, presumably, to a seasonally inimical environment. They consequently also undergo peri- odic "population explosions" as the environment becomes more favorable. We do not know of any studies of the radio- sensitivity of marine organisms under an ecologically mean- ingful range of conditions, both of environment and of growth rate. We must also consider whether the ecosystems of the open ocean may be themselves intrinsically more sensitive to increases of incident radiation. Radiation effects may be expressed in two ways: (a) di- rectly, by the irradiated organism, in a series grading from prompt lethality to reduced vigor, shortened life-span, and diminished reproductive rate; and (b) genetically, by the transmission to offspring of radiation-altered genes. Such altered genes are most commonly recessive and most com- monly disadvantageous to their carriers. It has been shown for Drosophila, however (Wallace and King, 1951; Wallace, 1956, 1958; Buzzati-Traverso, 1960), that heterosis pro- duced by accumulated radiation-produced mutations leads to significantly increased individual viability, even up to lev- els of accumulated mutations that result in a considerable frequency of genetic death. Rugh and Wolff (1958) have re- ported that radiation-induced mutations in mice may pro- duce increased resistance to radiation, again by heterosis. Comparable studies of several groups of microorganisms were noted by Buzzati-Traverso (1960), who emphasized that complex populations living competitively under radi- ation fields have not shown selection in favor of radioresis- tance genes. Styron (1969) recently studied two isolated populations of an aquatic isopod, one in an area of high natural gamma- ray background from extensive exposure of granite (Folsom and Harley, 1957); the population evolving under high radi- ation backgrounds ("several times the average for aquatic ecosystems") proved to have a 7.9 times greater tolerance to ionizing radiation, but the author did not claim this as evi- dence of selection for genes enhancing radiation resistance. Our ignorance of the genetic diversity within marine spe- cies still prevents any useful attempt to consider the genetic effects of increased radiation on pelagic ecosystems, al- though consideration of the histories of radiation exposure have long-term LDso's for 60Co irradiation of 215 and 300 rads, re- spectively-values quite like those exhibited by man. Examination of this question, they found, was further complicated, in the cases of Fundulus and ofArtemia salina, by a strong inverse correlation be- tween environmental salinity and radiation tolerance. See also Angelovic et al. (1969). of these ecosystems leads to the expectation that new sources of increase in the available gene pool should have beneficial effects for at least some species. Recent studies by Wallace (1966) and by Hoenigsberg (1968) emphasize the importance in this connection of the effective size of the gene pool. Hoenigsberg has shown that, in Drosophila species under wild conditions, gene pools may extend only over physical distances of 100 m or so and be represented by comparably small numbers of organisms. This clearly has very important implications for the fre- quency of elimination, by homozygosis, of recessive lethal mutations. We have emphasized the mobility of all pelagic populations and of a large fraction of the near-shore popu- lations as well. Studies by Scheltema (1966, 1967, 1968) have shown that the dispersal of planktonic larvae of many benthic species is an important source of recruitment of populations severely localized as adults and is also respon- sible for continual interchange of genetic material among separated local populations. The gene pools of marine species may, then, be expected to be characterized by large size, in terms of both physical extent and number of orga- nisms, and consequently by a slow rate of elimination of lethal genes. Such a situation would appear to optimize the beneficial effects of radiation-increased heterosis. There are two possible exceptions to this generalization: (a) those benthic organisms, both open-ocean and near- shore, that do not produce planktonic larvae and may be ex- pected to move only over very small distances; and (b) those planktonic species that undergo great seasonal fluctuations in abundance, with a consequent great reduction in genetic variability at each population minimum. Although this class of plankton appears to include a very large number of the most important pelagic primary producers (Hulburt, 1966; Menzel and Ryther, 1960), we do not appear to have enough information to estimate the minimum population at any sea- son or to judge to what degree physical mixing processes may be able to produce new genetic intermixing during the periods of rapid population increase. This would appear to be an important and fertile field for future study, both the- oretical and observational; its importance for our under- standing of the radioresistance of oceanic ecosystems is clearly large. We know of no data concerning the radiosensitivity of marine ecosystems as compared to that of the individuals within them. Fontaine (1960) pointed out that it is to be expected that the first effect on an ecosystem of a damaging radiation response by the most radiosensitive species in that ecosystem would be disequilibrium in "its community, a dis- equilibrium that clearly may have repercussions on human life outside the field of radioactivity." We know of no re- search that appears to have been directly stimulated by this suggestion. In fact, as discussed in Chapters 9 and 10 of this volume, the usual criteria for "acceptable" levels of radionu- clide release, or of environmental radionuclide concentra-

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212 Radioactivity in the Marine Environment A, CJ C< Co C. Fi Mn N. Pe. sn s• T. Z- z. 91V c: * e 5 5* r_ ^ ° i: n- en — .cj- ]- ci — ' — a FIGURE 1 Ranges of element concentration factors in marine or- ganisms at various trophic levels (data from Table 2). Log scale: 10'1 to 106; 104 marked by horizontal limit line. tion, are clearly homocentric, oriented toward questions concerning direct radiation exposure of man or of his pres- ent food organisms. It is concluded in Chapter 10 that a continuation of the policies and practices concerning the control of low-level waste disposal. . . established during these formative years should assure that radioactive con- tamination of the marine environment will not reach unac- ceptable levels. While it would be purely serendipitous if, in attempting to protect only man and the organisms he now exploits, the right decisions have been made with respect to protecting the ecology of the oceans as a whole, this appears in fact to have been the case. Man is among the most radiosensitive or- ganisms, and his greatest vulnerability to radiation lies in his genetic apparatus. Because we cherish the life of every hu- man being but are interested in preserving other organisms as populations rather than as individuals, our standards for the direct protection of man have also protected the pyra- mid of life in the sea, on which man ultimately depends. This conclusion is discussed further in Chapter 9. We believe, however, that information is available upon which to build a qualitative picture of the radiosensitivity of marine ecosystems; we believe further that our attempt in the following pages to build such a picture is appropriate to the present discussion. Klopfer (1959) suggested that four variables are princi- pally involved in determining the number of taxa in a given area: the time elapsed since colonization; the area's geo- graphic extent; its topographic variability; and its climatic variability. Of these, the first two would be expected, in the world ocean, to have favored development of a very large number of marine taxa. We believe that life originated in the oceans and that consequently the time for marine speciation has been the maximum available on earth; and, as we em- phasized earlier, the world oceans represent the longest en- vironmental continuum along which organisms can spread and differentiate. On the other hand, in ocean environments, the range of variability, either topographic or climatic, is probably small, compared to that in most large land areas. Contrary to Thorson's (1957) generalization, Hutchinson (1959) has noted that, in fact, marine environments (once account has been taken of the nonrepresentation therein of Insecta, Amphibia, and most orders of mammals) are char- acterized by greater species diversity than are those of land or fresh water. In spite of the enormous area represented by the oceans and in spite of the enormous time available for evolution within this area, such extensive diversity seems surprising in view of the very modest ranges of most of the environmental variables involved in niche determination. It appears that the diversity of marine species has been achieved by a long, slow evolution that has divided the en- vironment into a series of niches probably definable by vari- ations much more subtle than those that are critical in either land or freshwater determination. This conclusion appears to have significant implications with respect to the mechanisms of marine population con- trol. In a stimulating but controversial contribution, Hairston et al. (1960) concluded that (1) populations of producers, carnivores, and decomposers are limited by their respective resources in the classical density-dependent fashion, (2) interspecific competition must necessarily exist among the members of each of these three trophic levels, (3) herbivores are seldom food limited, appear most often to be predator-limited, and therefore are not likely to compete for common resources. In a related analysis, less simply theoretical and strictly ma- rine, Connell and Orias (1964) emphasized the role of avail- able energy in encouraging species diversity. They also con- cluded that the "instability of the medium" must discourage oceanic creatures from speciation into niches characterized by very rigorous physical, or presumably chemical, specifi- cations. As noted above, we believe that this argument does not apply to open-ocean plankton or benthon; we believe that even in the upper layers of water—those of maximum "instability"-the position in the environment of the various

Ecological Interactions of Marine Radioactivity 213 physically or chemically delimited niches must change, but that very few such niches would be seasonally or randomly obliterated. Some other conclusions reached by Connell and Orias are especially relevant, however, in the present context: Although some niches are determined by physical variations in the environment, most of the dimensions of the niche are a result of interaction between organisms. For this reason, it is impossible to predict the number of niches (and therefore species) from environmental complexity alone. We also dis- card the idea that rigorousness per se limits diversity. If these conclusions apply to the diversity of marine species, as we believe they do, the members of marine ecosystems might be expected to be more dependent on each other's productions and interactions than is true for members of land or freshwater ecosystems; the presence or products of other species may be the resources most commonly com- peted for. Equally, the need for specific products of a com- petitor species may be the factor preventing competition from resulting in complete displacement of one species by another. It seems likely to us that such considerations may be more important to planktonic than to benthic organisms. Kohn (1967) has shown that for Conus-a near-shore ben- thic gastropod genus-environmental complexity is the main source of species diversity. Radioactivity introduced into systems like these in dam- aging amounts may be viewed either as a "stress," which ap- pears analogous to environmental "rigorousness" as consid- ered by Connell and Orias (1964), or as an analogue of predation; the latter seems to be a more useful line to con- sider. As noted above, Hairston etal. (1960) concluded that only herbivores, as an ecological class, can be regarded as usually predator-limited. Murdoch (1966) has strongly criti- cized this view, and certainly it is more usual, we believe, to consider the aquatic herbivores as "resource-limited," with respect to food. Should herbivores, in fact, already be predator-limited, the introduction of a new "predator"— radiation damage—would directly reduce this population, and presumably as directly increase the fraction of primary productivity available for "decomposers," short-circuiting the food chain. At the same time, reduction of the herbivore population would, according to the argument of Hairston et al., reduce in parallel the resource-limited predator popu- lations. Of those trophic levels readily exploitable by man, only the detritus-feeders might be expected to profit from such a change. Of course, as the intensity of radiation pre- dation increased, an increasing number of species would be- come predation-limited, and radiation resistance would finally become the major criterion of interspecific com- petition. Following Slobodkin (1968), one may inquire whether, in this context, radiation damage is a "good" predator. Slobodkin considers "goodness" of predator behavior only from the predator's point of view—and, incidentally, con- cludes that predators generally "act as if they were behaving prudently." We have tried, however, to develop from his ar- gument an analogous "goodness" in terms of the biosphere: The yield of each species, in terms of conversion of its spe- cial set of raw materials to usable commodities, should be maximized, and the size of no species' population should be so reduced as to seriously diminish its ability to respond to disadvantageous fluctuations of the environment. From the viewpoint of the biosphere, the over-all "commodity" of the oceans might be taken as the maintenance of optimal O2 and CO2 levels in the atmosphere; this is clearly in the hands of the "primary producer" plants and of the carbonate skel- eton formers. All other species, in this view, would exist simply to ensure a smooth flow of nutrients to and catabo- lites from the primary producers and the carbonate formers and, following the argument of Connell and Orias (1964), to contribute to the "interspecific" fitness of their environ- ment. From such a point of view, radiation damage is an ex- ceptionally poor predator; it is not density-dependent and thus has no tendency to diminish its effect as a species ap- proaches the level of "reduced resilience." It tends to affect most seriously the young, fast-growing stages of the popu- lation—those of lowest "population efficiency," in Slobodkin's terms-whose loss both affects the resilience of the population and results in the poorest use of energy. Furthermore, unlike any other form of predation, it should tend finally to emphasize selection only for a variable of no other selection value at all, radiation resistance. It may be further argued that radiation predation would be especially dangerous for the planktonic species of the open sea: Most of these species undergo cyclic reductions to very low abun- dances, at which the population may not be able to with- stand further predation; these periods of low abundance are followed by periods of very rapid multiplication during which the radiosensitivity of individuals-by analogy with all experimental organisms so far studied—may be expected to increase in proportion to the rate of cell division. It appears possible also to argue that the more closely interdependent are the species of an ecosystem—and we be- lieve that those of marine environments are especially closely linked, and to a greater diversity of mutually inter- dependent species—the more especially radiosensitive will be the system. This argument critically depends on a wholly untested hypothesis-that the species interrelationships of marine ecosystems are specifically inflexible and that few (or no) participants in such an interrelationship can be re- placed by others. If this is so, then the group, when exposed to damaging radiation, would be limited by the response of its most sensitive members. This hypothesis, we believe, is supported by the types of marine species interactions listed

214 Radioactivity in the Marine Environment above (p. 205), as well as by the arguments of Connell and Orias (1964); it was also advanced by Fontaine (1960), on other grounds, some time ago. Support is also provided for this view by Imbrie's (personal communication) success in analyzing species abundance relationships in marine Fora- minifera populations (from sediments and from plankton), using a statistical procedure that required that the relative abundances of the individual species must always be the same in order to appear to vary as a group. If the relation- ship "species A needs species B needs species C needs spe- cies D" is quite inflexible, it would not be surprising to find, over considerable ranges of environment and of population abundance, that it could be quantitated as "10 individuals of species A need 6 of species B need 3 of species C need 2 of species D," and the relative abundance ranking of the species in the group would be maintained as the absolute abundances varied. On the other hand, if the relationship were "species A needs either species Bj, B2, or B3," then we would not expect B l, B2, or B3 to maintain a constant abundance relative to A as the absolute abundances vary. Techniques to explore whether this latter situation is at all common are presently being sought, but the fact that analy- sis based on the simpler situation has had success appears to confirm some cases of specifically inflexible interdepen- dences. It is clear that this sort of specifically inflexible interde- pendence would not act to increase stability of a community or ecosystem, contrary to the suggestions of MacArthur (1955) and Watt (1964) that increased stability would result from increase in the number of interspecies links. Paine (1969) has suggested that in quite different sorts of situ- ations-in ecosystems of moderate complexity (the inter- tidal community of the North American Pacific coast) or even of great complexity (the Great Barrier Reef off Aus- tralia)—the removal of one specific carnivore (among, in both cases, many other large carnivores) has resulted in ma- jor, even drastic (in the latter case), changes in the species composition of the whole system. Clearly, Paine's (1969) suggestions relate closely to that of Fontaine (1960), noted above, of the dependence of a linked ecosystem on the ra- diosensitivity of its most sensitive member. In conclusion, it appears that the patterns of cyclic abun- dance of many marine species are such as to make radiation damage especially serious when viewed as a form of preda- tion; it appears further that the patterns of interspecific mutual dependence inferred for marine ecosystems may have specifically reduced the ability of individual species to profit from higher levels of radioresistance. It does not ap- pear to us possible even to erect chains of argument that might relate this set of properties of marine ecosystems to those discussed earlier as probably making marine species more likely to show the stimulating effects of radiation- induced heterosis. The directions that should be taken by research in these areas are quite clear-as indeed they were when noted by Fontaine (1960) and Buzzati-Traverso (1960) at Monaco in 1959-but the actual experimental de- tails are mostly either obscure or of frightening complexity. Our hope in this discussion has been to point out how im- portant these problems are and to imply how unlikely it is that their practical solutions will be found in purely man- centered regulations. Again, however, let us reiterate that no support is intended for the view that present levels of ocean radioactivity, or any levels now contemplated, constitute significant ecological variables. HUMAN ECOLOGY AND THE MARINE ENVIRONMENT As man is an organism interacting with the oceans, his ecol- ogy is as suitable a subject for consideration here as that of any wholly marine species. Perhaps the most salient aspect of human ecology today, the "population explosion," clearly implies that there must be significant changes in man's relationships with the biosphere, as well as with his fellow man. Much recent discussion (Polikarpov, 1966, p. 233; President's Science Advisory Committee, 1966, Ch. 2; Butler and Holston, 1966; Iversen, 1967; Emery and Iselin, \967;Hydrospace, 1968; President's Science Advi- sory Committee, 1967; Schaefer, 1968) has dealt with the idea that increasing human needs for food can and will be met partially by expanded and more efficient exploitation of the organisms of the oceans. Such a change has clear and pertinent implications for our present consideration: Increasing the efficiency of exploitation of pelagic biota necessarily implies-if anything like an order-of-magnitude increase of efficiency is to be sought-that lower and lower trophic levels must be exploited; such exploitation carries with it the prospect of changes in the radionuclide exposure of the exploiters. Efficiency of exploitation can be greatly extended with safety only after significant growth of our understanding of the oceans as ecosystems. Marine radioactivity has been and is now a basic tool in extending this understanding, and the regulation of releases of radioactive materials to the marine environment should continue to be designed with this use in mind. As ecosystems, the oceans are continua to an extent not exhibited by any other systems subjected to human exploi- tation save the atmosphere, and like the atmosphere, the world ocean in something like its present ecological- geochemical dynamism is essential to life on earth. Consid- eration of the physical and biological histories of many areas in which the application of intensive agriculture predated reasonable knowledge of soil conservation—the deserts of

Ecological Interactions of Marine Radioactivity 215 Persia and North Africa or the semideserts of Spain and much of China, among others—shows how vital it is that ex- ploitation of the marine biota be intensified only hand in hand with full understanding of the importance to man of the intact ecosystem and of those variables critical to its continued integrity. These three problems are considered in greater detail in the following sections. Use of Lower-Trophic-Level Organisms in the Oceans as Food for Man As the earth's population increases, more attention will be directed toward the oceans as a source of human food. In terms of the efficiency of energy conversion and of deliber- ate attempts to cultivate and harvest the seas, the primary producers and the grazers become more and more appealing. Thus, grazers on plankton may become important foods for human consumption, supplementing the predaceous fish now largely in use, as well as the lower-trophic-level crusta- ceans and shellfish. This change of emphasis is a considera- tion of special force in aquatic environments, where food chains are typically of much greater length than are those on land. Polikarpov (1966, Ch. 12) concluded that in a uniformly labeled aquatic environment, radionuclides are more gen- erally accumulated directly from the water than indirectly by way of the food chain; he appears to have been strongly influenced in this view by studies of such radioelements as strontium and cesium. In studies of manganese metabolism by the lobster, Bryan and Ward (1965) have presented data indicating that most uptake must be from the animal's food; most of its zinc and copper, however, appears to be ab- sorbed directly from the water (Bryan, 1964). Studies of this kind have been made of few other organisms, and it does not appear to us that the available data support any firm generalization about paths of radioelement uptake. As Polikarpov points out, however, in a nonuniformly labeled environment, where organisms-cither prey or predators- migrate from higher to lower levels of radioisotope contami- nation, the food chain may be expected to be a major vari- able in an organism's accumulation of radioactivity. Data presented in Chapter 3 show that over very long periods of time after any radionuclide is introduced, and invariably for short-lived nuclides, nonuniform labeling of the marine en- vironment is precisely what will exist. As we have pointed out above, consideration of the energetics of ecosystems indicates that large increases in man's efficiency of exploitation of the marine biosphere for food can be made only by emphasizing increased use of grazers. If, as noted by Butler and Holston (1966), the em- phasis is on the oceans as a source of protein food—and lack of protein is notoriously the great dietary deficiency-then the grazers in the sea, as on land, are the most promising level for exploitation. Or if, as noted by Emery and Iselin (1967), man is approaching the point of diminishing returns in "gathering" or "hunting" food in the sea and must face the prospect of sea-farming—or, in their terminology, "herd- ing" of marine animals-there appears again more hope from exploitation of grazers. As Iversen (1967) pointed out, we know how to increase the food available to impounded crus- taceans or bivalves, as well as to "those fishes that feed low on the food web," but we do not know how to provide, cheaply or efficiently, food for impounded carnivorous fishes. Clearly, in this sort of situation, the position of scav- enger species that can exploit human wastes also deserves detailed consideration. In general, all roads to conclusions about large increases in "food from the sea" lead to increased use of grazing or- ganisms. And as the data of Table 2 suggest, this increase will be accompanied by increased intake of a large number of elements having important fission products or activation- produced radionuclides. If there is progressively increasing human use of marine grazing animals for food, accompanied by widespread marine disposal of radionuclide wastes, the problems of maintaining human exposure to radiation at low levels would be intensified. Use of the "specific-activity approach" to these problems (described in Chapter 10) de- pends on the assumption that man's present element con- centration levels would be maintained even in the face of significant changes in dietary concentration levels. For very few elements do we have good data in support of this as- sumption; on the other hand, we know of several (As, Sb, Te, Pb, to name a few) that man is unable to regulate; some implications of this uncertainty were considered in the 1962 National Academy of Sciences-National Research Council pub\ication, Disposal of Low-Level Radioactive Wastes into Pacific Coastal Waters. Furthermore, the history of regula- tory activities is one of very slow response to increased haz- ards resulting from technological change. This is well illus- trated by consideration of the histories of the use of lead in interior paints, of automobile design and traffic control, of the use of fossil fuels in urban environments, and so on. That the Windscale and other British releases of radioactive waste have been constantly, and thoughtfully, re-evaluated and controlled (Preston and Jefferies, 1969) is a great credit to the agencies responsible, but this is only a small ray of hope in the largely gloomy history of industrial pollution. Whatever the approach used—"specific activity" or "critical pathway" (see Chapter 10)-there will exist a clear opportunity for neglect of those changes in regulations im- plied by alteration of man's dietary emphases. In the specific-activity approach, the probability that much of the change in exposure to man may be in increased gut-content levels is coupled with the explicit neglect of synergism be-

216 Radioactivity in the Marine Environment tween exposures to the gut and to the "critical organ" esti- mated from stable element distribution. In the critical- pathway approach, the likelihood that new critical pathways will appear for each radionuclide as human food emphasis shifts to lower trophic levels puts on the regulatory agency an onus of constant resurvey of each disposal situation. It appears clear to us that at any given level of radioactivity in the oceans, both the hazards to man and the problems of guarding populations against these hazards will necessarily be greater, and possibly a good deal greater, if he is eating grazing organisms than if he is eating predators. The statis- tics of published information on critical-pathway control situations are in agreement with this view. Two other consequences of importance in this context would follow man's placing greater reliance on grazers or first-stage predators drawn from the pelagic environment for food: (a) the organisms eaten would, in general, be of smaller size and consequently of greater surface: volume ratio than most of those now exploited; and (b) even be- yond this purely geometrical increase in surface: volume ratio, the organisms of the plankton have tended to evolve bodies having extra-large surfaces, whether to enhance gas exchange, to resist sinking, or as an adjunct to food gather- ing. Moreover, as food-organism size diminishes, man's ten- dency to consume the whole organism increases, for in- stance, sardines, fish meal, or even the often-advocated plankton paste. From foods of this sort, man would be ef- ficiently exposed not only to the amount of radionuclide concentrated by the organism, as indicated by its analytical concentration factors, but also to the amounts held in its gut from recent meals and to that adsorbed on its external sur- faces. Studies summarized by Lowman (1960) have shown that many radioactive nuclides appear at higher concentra- tion ratios in gut contents or adsorbed on surfaces than they do in the metabolic cycles of plankton organisms. Already, both dietary preference and economic factors have led large fractions of the world population to the con- sumption of whole marine organisms, including shell; the small dried shrimp used widely in the Orient and in Brazil and the shrimp-flour chips that have spread from Indonesia to very wide use in South America and elsewhere offer ex- amples of this. An amusing aspect of the variability of human ecology, in the sense of feeding habits, appears as a consequence of Ward's (1966) study of the uptake and distribution of plu- tonium in the lobster. Her conclusion is, implicitly, that be- cause 90 percent of the 239Pu taken up by Homarus vulgaris is deposited in the calcified shell, the lobster as a dietary vector of Pu can be taken as minimized. This is clearly rea- sonable for those who ingest the organisms in cocktails, salads, or otherwise from the shell; it is not so, however, for those gourmets addicted to lobster bisque-a soup thickened by a paste of pounded lobster shell. Since one can reason- ably predict similar Pu concentration in the shells of other edible crustaceans, and since crab bisque, shrimp bisque, and crayfish bisque are of comparable elegance, one can envision a dichotomy of radionuclide hazard based on gastronomic sophistication. Since we are here considering human ecology, it is ap- propriate to mention the very extensive literature-largely in Japanese-concerning the use of drastically "modified" marine organisms as food, in the forms offish pastes, "cheeses," sausage, and the like. Much of this work appears to have been motivated by a desire to retrieve materials stored too long rather than by a striving for gastronomic elegance. However, the modification procedures point to- ward ways of producing edible protein of much lower radio- nuclide content, as well as toward lowering the content of toxic or unpalatable decomposition products, toward which this work was aimed. That such processing would result in increased costs appears self-evident, but that it could be done without unbearable economic results in case of persis- tent need for radionuclide decontamination is as likely as that it would-as it has in Japan-prove cheaper to reprocess fish than to store them at low temperatures. Man's techno- logical dexterity and his ability to find its results acceptable are among his most salient adaptive traits. Considerable interest attaches to the time scale of man's increasing demand for food. From Butler and Holston (1966), it appears that the United Nations is thinking in terms of supplying from the sea about 20 percent of the world demand for animal protein—estimated values vary from 14 g per capita per day (Butler and Holston, 1966) to 15-20 g per capita per day (Schaefer, 1968, and personal communication), a maximum requirement for 3 X109 peo- ple of 22 X109 kg of animal protein per year. In 1964, the world ocean yielded (Emery and Iselin, 1967) 28.6 X106 tons of animals for human food—roughly equivalent to 5 X109 kg of animal protein; this represented, then, almost 25 percent of the estimated maximum requirement for a world population of three billion, if properly distributed. As both Emery and Iselin and Butler and Holston imply, the ocean's yield of human food could have been approximately doubled simply by using the marine food now fed to domes- tic animals or used as fertilizer. Butler and Holston con- cluded that present annual harvests of marine animals could be increased fivefold to tenfold by fairly straightforward im- provements of present harvesting, but that this represents a ceiling above which further increase in harvesting can be achieved only by an emphasis on trophic levels lower than those now exploited. Schaefer (1968), however, pointed out that as much as 40 percent of the 1964-1968 world fishery harvest was represented by "herring-like fishes" feeding at the first or second trophic level above the planktonic plants. Although this did not offer encouragement that large gains in fishery yield would come from transfers of effort to still lower trophic levels, Schaefer's calculations of "probable potential yield" of the world ocean (based on estimates of

Ecological Interactions of Marine Radioactivity 217 total net primary productivity of the oceans, and 10 to 20 percent per trophic-level transfer coefficient) indicate that the marine fishery should be capable of supplying (without change in trophic-level emphasis) one to six times the total protein requirement of a world population of six billion people—double that of the present. Schaefer further estimated that, based on technical considerations, about a fivefold increase of the world fishery harvest could be achieved "with no radical developments, such as fish farm- ing." It may then be concluded that while there are basic disagreements about the reasons, there is some agreement about the conclusion that by the time a fivefold to tenfold increase has been achieved in the protein harvest of the oceans, either trophic-level considerations or considerations of harvesting technique will cause greater emphasis to be placed on the use as food of lower-trophic-level fishes and invertebrates (Butler and Holston, 1966) or on those marine animals susceptible to economic "sea farming" [lower- trophic-leyel fishes and invertebrates again, as Iversen (1967) concluded]. This appears from both Butler and Holston and Schaefer to be projectable to the last decades of the present millenium—1980 to 2000. It is, then, not too soon to engage in speculation on the consequences of massive (or of more massive) exploitation of marine grazers. Man's present low level of dependence on marine sources of food, combined with his present practice of using princi- pally the higher trophic levels in his diet, has given added as- surance that the permissible concentrations of radionuclides in ocean water (as given by the National Academy of Sciences-National Research Council, 1962, for example) are conservative. As human populations grow, with rapidly increasing demands for animal protein, it will become de- sirable to significantly increase our exploitation of marine biota. Consideration either of the energetics of food webs or of the technology of animal "aquiculture" has led us to conclude that sizable increases in marine food supply must be made by utilizing grazing animals, as has been true on land for the same reasons. Analytical data show, however, that marine grazers tend to have larger concentrations of radionuclides than do the marine predators now largely ex- ploited. Thus, the future seems to indicate that man's in- creasing need for protein will tend to reduce his emphasis on one or two links in the food chain that may have pro- vided an extra degree of insulation from the radioactivity in the sea. As the National Academy of Sciences-National Research Council (1962) noted, much of the basic data con- cerning the elemental composition of marine food organisms and man's assimilation and retention of elements from such food was lacking. This is still true. We hasten to add that either the specific-activity ap- proach or the critical-pathway approach, when properly ap- plied and continually adjusted as the environmental situa- tion changes, will ensure that the concentrations of radionuclides in our diet, regardless of what seafood we eat, will be below permissible levels. Extensive long-term studies of food organisms from the Irish Sea near Windscale and from the northeast Pacific Ocean off the Columbia River indicate that the health and safety of human beings has been a primary consideration in release limits of radionuclides. Marine Radioactivity as a Basic Research Tool in Ecology The tracer experiment provided to scientists by the two periods of intense atmospheric testing of nuclear explosives offered a unique opportunity to explore details, especially of rates of transfer, of marine geochemistry and hydrog- raphy. These tracers are discussed both in Chapter 3 and in sections concerned with circulatory processes in Chapter 4. However, even after fifteen years we still have not learned how this tracer experiment may best be exploited. It must be emphasized that the "fallout tracer experiment" itself seriously affected our ability to profit from other tracer ex- periments. Tritium, for example, is a "natural" radionuclide in addition to being a major product of thermonuclear de- vices. It is continuously being produced, at low but measur- able levels, by cosmic ray processes in the atmosphere. The existence of this natural tritium as a geochemical and mete- orological tracer was predicted by Libby in 1946; publica- tion of data confirming this promise began in 1951 (Grosse era/., 1951). In 1952, the United States carried out its first thermonuclear explosion, and by 1954, the Castle series of weapons tests had introduced artificial tritium to levels that overwhelmed the natural levels. By contrast, the first sub- surface seawater samples were collected for tritium analysis in September 1954 (Begemann and Libby, 1957); the only pre-Castle surface-water samples were collected in late 1952, and these were very few in number. Not merely has our abil- ity to use the data resulting from the introductions of ther- monuclear tritium been diminished by our ignorance of pre- Castle tritium concentrations, but our opportunity to observe the profiles of equilibrium concentration levels of natural tritium was destroyed before it could be taken. Ex- tremely valuable oceanographic information could have been obtained through estimation of the speed at which the bomb-introduced tritium approached the equilibrium profile of natural concentrations. The same test series also disrupted our use of natural carbon-14 as a long-lived tracer for study of many of the same processes as those in which tritium is involved. In fairness, however, it should be stated that the develop- ment of sensitive counting equipment essential to tracer studies was greatly accelerated by the nuclear testing program. The oceans must be studied as a single intact ecosystem. Above (p. 200), we noted one type of bar to their easy

218 Radioactivity in the Marine Environment exploration, but there are many others. Large-scale tracer experiments may be the only way by which some parame- ters can be evaluated well enough to support the kind of model-system studies that we believe are required to evalu- ate plans for new ways to exploit the marine environment. Our use of such large-scale tracer experiments to achieve understanding of the marine ecosystem could be hampered if radioactivity concentrations in seawater are very much lower than the levels that would affect our present ability to exploit the system. Plans for any massive new introductions of radioactivity into the oceans must be evaluated in the light of, among other things, the possibility of premature in- terruption of the tracer experiments now in progress. The Significance to Man of the Oceans as a Functioning Ecosystem It has been common for man to assume that any space is relatively large compared to his own dwelling—and this seems to apply as well to air-shafts in slum apartments as to streams, rivers, lakes, marshes, the atmosphere, and the oceans-and can be used as a waste depository. The hazards of this approach have become clear in the case of streams, rivers, and lakes, and locally in the case of the atmosphere; it has even become clear that each ecosystem may have a characteristic half-time for recovery from such abuse and that this interval is longer as the system in question is larger—i.e., longer for a river than for a stream, or for a lake than for a pond—and longer as it is more sluggish—i.e., longer for a pond than for a stream or for a lake than a river. All our knowledge of the oceans promises that, once seriously insulted in an ecological sense, their recovery would be slow indeed. It is most fortunate that the philoso- phy of nuclear waste disposal has so far been enlightened in this respect. It is important to emphasize, among the many reasons for continued adherence to today's enlightened phi- losophy, the fact that the oceans represent the fraction of the earth's surface exhibiting a positive O2 balance versus the atmosphere and controlling the CO2 balance. Man must maintain the world ocean as a functioning ecosystem for this reason, even if there were no others. SUMMARY Lower trophic levels of the seas are likely to have greater concentrations of radioactivity than higher trophic levels. If the population explosion forces man to use these lower trophic levels as food sources, then the capacity of the seas to safely accept waste radioactivity will decrease. If, as suggested, marine species are both more closely linked than those of other ecosystems, and if unique—or very limited—species interdependences are here more com- mon, then the radiation resistance of marine ecosystems will often be strongly limited by that of the least resistant spe- cies. No marine radioactivity levels have yet approached possible danger points, but this is argued as one of several aspects of the oceans needing fuller consideration in these contexts. In order to assess properly the consequences to man of radioactivity in the marine environment, continued research is needed into the physics, chemistry, and biology of the oceans and into the interdisciplinary "hyphenated" off- spring of these basic sciences. Of particular importance is in- creased research into the radiosensitivity of marine ecosys- tems. 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220 Radioactivity in the Marine Environment Iversen, E. S. 1967. Farming the sea. Oceanol. Int. May/June: 28-30. Jennings, C. D. 1968. Iron-55 in Pacific Ocean organisms. Ph.D. thesis. Oregon State Univ., Corvallis. Jones, R. F. 1960. The accumulation of nitrosyl ruthenium by fine particles and marine organisms. Limnol. Oceanogr. 5(3): 312-325. Ketchum, B. H., and V. T. Bowen. 1958. Biological factors determin- ing the distribution of radioisotopes in the sea, p. 429-433. In Proceedings of the second international conference on the peace- ful uses of atomic energy, Geneva, 1958. Vol. 18. UN Publ., New York. Klopfer, P. H. 1959. Environmental determinants of faunal diversity. Amer. Natur. 93:337-342. Kohn, A. J. 1967. Environmental complexity and species diversity in the gastropod genus Conus on Indo-West Pacific reef platforms. Amer. Natur. 101:251-259. Kuenzler, E. J. 1969a. Elimination of iodine, cobalt, iron and zinc by marine zooplankton, p. 462-473. In D. J. Nelson and F. C. 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Curl, Jr. 1963a. Acceleration of sinking rates of radionuclides in the ocean. Nature (London) 200:1276-1277. Osterberg, C., W. G. Pearcy, and H. Curl, Jr. 1964. Radioactivity and its relationship to the oceanic food chains. J. Mar. Res. 22(1):2- 12. Osterberg, C., L. Small, and L. Hubbard. 1963b. Radioactivity in large marine plankton as a function of surface area. Nature (London) 197:883-884. Paine, R. T. 1969. A note on trophic complexity and community stability. Amer. Natur. 103(929):91-93. Pearcy, W. G., and C. L. Osterberg. 1967. Depth, diet, seasonal and geographic variations in zinc-65 of mid-water animals off Oregon. Int. J. Oceanol. Limnol. 1(2): 103-116. Phelps, D. K., R. J. Santiago, D. Luciano, and N. Irizarry. 1969. Trace element composition of inshore and offshore benthic populations, p. 509-526. In D. J. Nelson and F. C. Evans [ed.] Symposium on radioecology. CONF-670503. USAEC, Oak Ridge, Tenn. Polikarpov, G. G. 1966. Radioecology of aquatic organisms. 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Economic and social needs for marine re- sources, p. 6-37. In J. F. Brahtz [ed.] Ocean engineering. Wiley, New York. Scheltema, R. S. 1966. Evidence for transatlantic transport of gas- tropod larvae belonging to the genus Cymatium. Deep-Sea Res. 13:83-95. Scheltema, R. S. 1967. Significance of larvae to the zoogeography of shoal water tropical benthos, read at the conference on marine invertebrate larvae, Beaufort, N.C., 1967. Scheltema, R. S. 1968. Dispersal of larvae by equatorial ocean cur- rents and its importance to the zoogeography of shoal water tropical species. Nature (London) 217:1159-1162. Schultz, V., and A. W. Klement, Jr. [ed.]. 1963. Radioecology. Reinhold, New York. 746 p. Seymour, A. B., and G. B. Lewis. 1964. Radionuclides of Columbia River origin in marine organisms, sediments and water collected

Ecological Interactions of Marine Radioactivity 221 from the coastal and offshore waters of Washington and Oregon, 1961-1963. Univ. Washington, Seattle, Laboratory of Radiation Biology, Rep. UWFL-86. 73 p. (With data appendix, p. 1-40.) Slumi/ii. T. 1967. Annual fluctuations of several inorganic elements in shortneck clams. Nippon Suisan Gakkaishi 33(7):686-689. Slobodkin, L. B. 1968. How to be a predator. Amer. Zool. 8:43-52. Slowey, J. F., D. Hayes, B. Dixon, and D. W. Hood. 1965. Distribu- tion of gamma emitting radionuclides in the Gulf of Mexico, p. 109-129. In D. R. Schink and J. T. Corless [ed.] Sympo- sium on marine geochemistry. Univ. Rhode Island Occasional Publ. 3. Spencer, D. W. 1968. A stochastic model of nickel in the Atlantic Ocean. Presented at A.G.U., Washington, D.C., April. Stephens, G. C. 1968. Dissolved organic matter as a potential source of nutrition for marine organisms. Amer. Zool. 8(1):95-106. Styron, C. E. 1969. Ecology of two populations of an aquatic isopod (Lirceus fontinalis Raf.) with emphasis on ionizing radiation ef- fects, p. 53-60. In D. J. Nelson and F. C. Evans [ed.] Sympo- sium on radioecology. CONF-670503. USAEC, Oak Ridge, Tenn. Tamotsu, M., M. Satake, J. Yamamoto, and S. Harona. 1964. On the microconstituent elements in marine invertebrates. J. Oceanogr. Soc. Japan 20:117-121. Thorson, G. 1957. Bottom communities. In Treatise on marine ecol- ogy and paleontology. Vol. 1. Geol. Soc. Amer., Mem. 67:461- 534. Ting, R. Y., and R. deVega. 1969. The nature of the distribution of trace elements in long nose anchovy (Anchoa lamprotaenia Hild.), Atlantic Thread herring (Opisthonema ogiinum LaSueur), and alga (Udotea flabellum Lam.), p. 527-534. In D. J. Nelson and F. C. Evans [ed.] Symposium on radioecology. CONF-670503. USAEC, Oak Ridge, Tenn. United Nations. 1958. Proceedings of the Second International Con- ference on Peaceful Uses of Atomic Energy, Geneva, 1958. 22 vol. New York. Vinogradova, Z. A., and V. V. Kovalskiy. 1962. Elemental composi- tion of the Black Sea plankton. Dokl. Akad. Nauk SSSR 147:217-219. Wallace, B. 1956. Studies on irradiated populations of Drosophila melanogaster. J. Genet. 54:280-293. Wallace, B. 1958. The average effect of radiation-induced mutations on viability in Drosophila melanogaster. Evolution 12:532-556. Wallace, B. 1966. Distance and the allelism of lethals in a tropical population of Drosophila melanogaster. Amer. Natur. 100:565- 578. Wallace, B., and J. C. King. 1951. Genetic changes in populations under irradiation. Amer. Natur. 85:209-222. Ward, E. E. 1966. Uptake of plutonium by the lobster, Homarus vulgaris. Nature (London) 209:625-626. Watt, K. E. F. 1964. Comments on fluctuations of animal popula- tions and measures of community stability. Can. Entomol. 96:1434-1442. Watt, K. E. F. 1968. Ecology and resource management: A quanti- tative approach. McGraw-Hill, New York. 450 p. Wooster, W. S., and J. H. Jones. 1966. Frontal studies with in situ salinometer. Paper presented at Second Int. Oceanogr. Congr., Moscow, May. Yermolayeva-Makovskaya, A. P., L. A. Pertsov, and D. K. Popov. 1968. Polonium-210 in the human body and in the environment. Acad. Sci. USSR Rep. to UN Sci. Comm. Eff. At. Radiat. A/AC.82/G/L.1260. 8 p. Young, E. G., and W. M. Langille. 1958. The occurrence of inorganic elements in marine algae of the Atlantic Provinces of Canada. Can. J. Bot. 36:301-310. BIBLIOGRAPHIC NOTE AND UPDATING REFERENCES No substantial updating of literature references has been possible since about mid-1969. Attention should be drawn especially to the Symposium on Radioecology (Proceedings of the Second National Symposium, Ann Arbor, May, 1967), edited by D. J. Nelson and F. C. Evans (CONF-670503. USAEC, Oak Ridge, Tenn. 774 p; available from the Na- tional Technical Information Service, Springfield, Va. 22151). Only a few of many pertinent papers in this volume could be specifically referred to in this chapter. Also pertinent are the following: Aarkrog, A. 1971. Radioecological investigations of plutonium in an arctic marine environment. Health Phys. 20(l):31-47. Angelovic, J. W., and D. W. Engel. 1970. Effects of radiation on es- tuarine organisms. Mar. Pollut. Bull., N.S. 1(7): 103-105. Angelovic, J. W., and J. C. White, Jr., and E. M. Davis. 1969. Inter- actions of ionizing radiation, salinity and temperature on the es- tuarine fish, Fundulus heteroclitus, p. 131-141. In D. J. Nelson and F. C. Evans [ed.] Symposium on radioecology. CONF- 670503. USAEC, Oak Ridge, Tenn. 774 p. Aten, A. H. W., Jr. 1961. Permissible concentrations of radionuclides in sea water. Health Phys. 6:114-125. Blackmore, D. T. 1969. Studies of Patella vulgata L. II. Seasonal variation in biochemical composition. J. Exp. Mar. BioL Ecol. 3:231-237. Bowen, V. T., K. M. Wong, and V. E. Noshkin. 1971. Plutonium 239 in and over the Atlantic Ocean. J. Mar. Res. 29(1): 1-10. Bryan, G. W. 1969. The absorption of zinc and other metals by the brown sea weed Laminaria digitata. J. Mar. Biol. Ass. U.K. 49(l):225-244. Chapman, W. H., H. L. Fisher, and M. W. Pratt. 1968. Concentration factors of chemical elements in edible aquatic organisms. USAEC Research and Development Report UCRL-50564. 50 p. (also TID-4500, UC^8.) Chipman, W., and J. Thommeret. 1970. Manganese content and the occurrence of fallout 54Mn in some marine benthos of the Medi- terranean. Bull. Inst. Oceanogr. Monaco 69(1402): 1-15. (Also Radioactivity in the sea, IAEA Publ. No. 28.) Cross, F. A., S. W. Fowler, J. M. Dean, L. F. Small, and C. S. Osterberg. 1968. Distribution of 65Zn in tissues of two marine crustaceans determined by autoradiography. J. Fish. Res. Bd. Can. 25(11):2461-2466. Gushing, C. E., and D. G. Watson. 1968. Accumulation of 32P and 65Zn by living and killed plankton. Oikos 19(1):143-145. Evans, E. A., H. C. Sheppard, and J. C. Turner. 1970. Validity of tritium tracers. Stability of tritium atoms in purines, pyrimidines, nucleosides and nucleotides. J. Labelled Compd. 6(l):76-87. Fowler, S. W., and L. F. Small. 1967. Moulting of Euphausia pacifica as a possible mechanism for vertical transport of zinc-65 in the sea. Oceanol. Limnol. l(4):237-245. Fujita, T., T. Yamamoto, I. Yamazi, and T. Shigematsu. 1969. Chemical studies of marine plankton. Ash, iron and manganese contents in marine plankton. Nippon Kagaku Zasshi 90(7):680- 686. Fukai, R. 1968. Some biogeochemical considerations on the radio- active contamination of marine biota and environments, p. 391- 394. In Proceedings of the First International Congress on Radi- ation Protection. Pergamon, Oxford.

222 Radioactivity in the Marine Environment Giese, A. C., and M. A. Hart. 1967. Seasonal changes in component indices and chemical composition in Katharina tunicata. J. Exp. Mar. Ecol. 1(1):: 34-46. Hibiya, T., and M. Oguri. 1961. Gill absorption and tissue distribu- tion of some radionuclides (s iCr, 203Hg, 65Zn and i 10mAg) in fish. Bull. Nippon Suisan Gakkaishi. 27:996-1000. Hobden, D. J. 1969. Iron metabolism inMytilusedulis II. Uptake and distribution of radioactive iron. J. Mar. Biol. Ass. U.K. 49(3):661-668. Ichikawa, R. 1961. On the concentration factors of some important radionuclides in the marine food organisms. Nippon Suisan Gakkaishi. 27:66-74. Ikuta, K. 1968. Studies on the accumulation of heavy metals in aquatic organisms. II. Accumulation of copper and zinc in oys- ters. Nippon Suisan Gakkaishi. 34(2):112-116. Ikuta, K. 1968. Studies on the accumulation of heavy metals in aquatic organisms. III. On accumulation of copper and zinc in parts of oysters. Nippon Suisan Gakkaishi. 34(2): 117-122. Jenkins, C. E. 1969. Radionuclide distribution in Pacific salmon. Health Phys. 17:507-512. Mitchell, R., and H. W. Jannasch. 1969. Processes controlling virus inactivation in sea water. Environ. Sci. Technol. 3(10):941-943. Naidu, J. R., and A. H. Seymour. 1969. Accumulation of zinc by oysters in Willapa Bay, Washington, p. 463-474. In Proceedings of the symposium on mollusca, Part II. Bangalore Press, Banga- lore, India. Ozvetic, B., S. Keckes, and C. Lucu. 1968. Sensitivity of the early developmental stage to U.V. in the sea urchin. (Abstr.) Rapp. Proc. verb. Comm. Int. Exp. Sci. Mer Mdditer. 19(2):195. Parekh, J. M., S. T. Talreja, B. J. Bhalela, and Y. A. Doshi. 1969. Scavenging of nuclear fission products by sea weeds from sea water. Current Sci. (India) 38(13):308-310. Preston, E. M. 1971. The importance of ingestion in chromium-51 accumulation by Crassostrea virginica (Gmelin). J. Exp. Mar. Biol. Ecol. 6(l):47-54. Raines, G. E., S. G. Bloom, and A. A. Levin. 1969. Ecological models applied to radionuclide transfer in tropical ecosystems. Bioscience 19(12):1086-1091. Rozhanskaya, L. I. 1968. Manganese, copper and zinc in the plank- ton, benthos and fishes of the Sea of Azov. Oceanology (USSR) 8(6):803-807. Scheltema, R. S. 1971. Larval dispersal as a means of genetic ex- change between geographically separated populations of shallow water benthic marine gastropods. Bio. Bull. 140:284-322. Small, L. F. 1969. Experimental studies on the transfer of 65Zn in high concentration by euphausiids. J. Exp. Mar. Biol. Ecol. 3:106-124. Somen, S. D., V. K. Penday, K. T. Joseph, and S. J. Raut. 1969. Daily intake of some major and trace elements. Health Phys. 17(1): 35-10. Strohal, P., S. Lulic, Z. Kolar, O. Jelisavcic, and S. Keckes. 1969. Gamma spectrometric analyses of some North Adriatic organ- isms. Rapp. Comm. Int. Mer Mdditer. 19(5): 95 3-95 5. Thomas, C. W., D. L. Reid, and L. F. Lust 1958. Radiochemical analysis of marine biological samples following the "Redwing" shot series. USAEC Research and Development Report HW 58674. 82 p. Ting, R. Y. 1969. Use of stable element distribution patterns for predicting distribution of radionuclides in marine organisms. Bioscience 19(12): 1082-1085. Vaughan, B. E., and J. A. Strand. 1970. Biological implications of a marine release of 90Sr. Health Phys. 18:25-41. Wong, K. M., V. E. Noshkin, L. Surprenant, and V. T. Bowen. 1970. Plutonium 239 in some marine organisms and sediments. U.S. Atomic Energy Commission, Health and Safety Laboratory, Fall- out Program Quarterly Summary Program, HASL-227:I-25-I-33. Wong, K. M., J. C. Burke, and V. T. Bowen. 1971. Plutonium con- centrations in organisms of the Atlantic Ocean. Health Phys. in press. Zlobin, V. S. 1968. The dynamics of radiostrontium uptake by some brown algae and the effect of the salinity of sea water on the concentration factors. Oceanology (USSR) 8(l):60-66.

Chapter Nine RADIATION EFFECTS W. L. Templeton, R. E. Nakatani, E. E. Held Under the present expansion in the development of nuclear energy, it is inevitable that the marine environment will con- tinue to receive an increasing burden of radiation. We must therefore be concerned with the amounts and kinds of radi- ation the individual organism, the population, and the eco- system can tolerate without significantly changing the "bal- ance of nature." This balance is not static; it responds to a multiplicity of factors, both natural and man-made. Radi- ation is but one of these factors. However, irradiation is not a recent introduction to the marine environment, since low levels of radiation from environmental and cosmic sources have been present to varying degrees throughout geological time. Our knowledge of the responses of ecosystems to small changes in their components is extremely limited; and, furthermore, the interactions of elements of the natural en- vironment have yet to be explored. All types of ionizing radiations produce changes in living cells, and some changes, at least, are regarded as deleterious. Until we learn otherwise, it is assumed that any radiation ex- posure in excess of the "natural" level might produce dele- terious changes. The biological consequences of low-level irradiation have grown, therefore, into a subject of impor- tance in all environments. Our knowledge of this subject with respect to the marine environment is still extremely limited and is mainly concerned with somatic effects. The potential hazards to man of radiation exposure have been and are being studied very extensively. In general, the conclusion from these studies is that any significant increase in radiation levels is detrimental from the genetic point of view. However, for man, this acceptance rests on ethical con- siderations with respect to the individual and on the fact that genetic anomalies are not reparable in an individual. When considering the marine environment, however, we are not primarily concerned with individual organisms, but with populations, and at the population level genetic damage is reparable by natural selection. This conclusion is summed up clearly in a paper by Purdom(1966). It would seem likely that the genetic response of popula- tions is relatively unimportant and that general mortality and infertility would be the limiting factors in the extent to which populations may overcome radiation exposure. This certainly seems true for animals which have been studied ex- tensively— Drosophila, the mouse, and domesticated farm animals. Provided that marine organisms are not more sensi- tive genetically than these other organisms, genetic damage will probably have negligible effects, even under the maxi- mum radiation exposures that seem possible from present day practice. In Chapter 2 are described those sources that release ra- dionuclides into the environment. In Chapters 3 through 8 the physical, chemical, and biological factors that determine the distribution of the radionuclides are discussed. Some ra- dionuclides remain in solution or suspension in the seawater, and some find their way into sediments, both sources con- tributing to the dose to organisms. Other nuclides will be 223

224 Radioactivity in the Marine Environment TABLE 1 Radiation Dose Rates in mrad/Week in Various Tissues of Cod (Gadus callarias) and Haddock (Gadus aeglefinus), from the Decay of 40K and 226Ra" Cod Haddock Radionuclide Muscle Skin Bone Fins Muscle Skin Bone Fins 40K (3 1 0.43 0.25 0.28 0.16 0.03 0.01 0.01 0.01 0.36 0.25 0.32 0.03 0.01 0.02 0.16 0.01 226Ra 0.020 0.040 - "After Fedorov (1965). TABLE 2 Estimates of Natural-Radiation Dose Rates to Plaice (Pleuronectes platessd) in the Irish Sea" Source Type of Radiation Dose in mR/week Natural activity in seawater (40K only) Natural activity in seabed (estimate) Cosmic radiation at 20 m 40K in fish Total 7 (3 1 0 0.07 0.18 1.00 0.10 0.01 0.22 1.58 mR/week or 0.082 R/year "Data from Woodhead (personal communication). absorbed by organisms or adsorbed on their surfaces; these nuclides will contribute to the internally delivered dose to a greater or lesser extent, depending on the size and complex- ity of the organism and the energy of the emission. In ad- dition, any of the parameters discussed in Chapter 7 or any group of them influences the exposure of organisms to radiation. Laboratory studies of radiation effects on individuals have been made with a variety of techniques. The basic studies of sensitivity to acute doses of radiation have mainly employed x rays, while studies attempting to reflect the en- vironmental conditions have used 60Co and 137Cs sources or radionuclides in solution. Environmental and population studies have been more limited, however. Our intention in this chapter is to consider only that re- search pertinent to the prediction of what might occur in the marine environment; therefore, we have not considered all of the studies that have been carried out using marine or- ganisms in radiobiological research. NATURAL RADIOACTIVITY The sources contributing to the natural background radia- tion dose of organisms in the marine environment are cosmic rays and the natural radioactivity in the earth's crust, pres- ent in seawater sediments and biota (Folsom and Harley, 1957). More than 60 radionuclides have been identified within the marine ecosystem (Chapter 2), and, based on these measurements, some calculations have been made of the dose rates to which the biota is exposed. Cherry (1964), in studies with phytoplankton from the open sea, shows that dose rates from total alpha activity in organisms could range from 230 mR/yr to 2.8 R/yr. Fedorov (1965) has calculated the tissue dose from 40K and 226Ra in cod, Gadus callarias, and in haddock, Gadus aeglefinus (Table 1). Estimates have been made (Ministry of Agricul- ture, Fisheries and Food, 1967) of the beta and gamma dose rate from the environment to the predominantly bottom- living plaice, Pleuronectes platessa, in the Irish Sea (Table 2). The major source of radiation as far as this species of fish is concerned is the seabed. Recent measurements of 210Po in marine organisms sug- gest that radiation from natural alpha emitters contributes significantly to the radiation dose to organisms (Beasley, 1968). MORTALITY INDUCED BY ACUTE RADIATION EXPOSURE Lethal amounts of acute radiation differ widely among or- ganisms because of biological variations related to such fac- tors as species, age, physiological state, and body size. In the aquatic environment, these variations are further compli- cated by the interaction of environmental factors such as temperature, dissolved oxygen, chemical composition, and salinity. Nevertheless, exclusive of the eggs and larvae of in- vertebrates and fish, most of the freshwater and marine or- ganisms for which data exist are relatively radioresistant.

Radiation Effects 225 Marine species differ little in radiation tolerances from freshwater species. Values of LD50 (lethal dose resulting in 50 percent mor- tality) for acute irradiation of aquatic organisms have been listed by Donaldson and Foster (1957) and by Polikarpov (1966). In general, there is a relationship between radiore- sistance and the phylogeny and ontogeny of the organism. Primitive forms are more resistant than the complex verte- brates, and older organisms are more resistant than the young. Bacteria and algae may tolerate doses of thousands of roentgens, but freshwater fish, the most sensitive group listed by Donaldson and Foster (1957), were affected by considerably lower doses. The LD50 for adult rainbow trout, Salmogairdneri, ranged from 300 to 3,000 R; and for the most sensitive stage of a developing trout egg, the LD5O value was as low as 16 R. Despite research into lethal effects of radiation for over 50 years, surprisingly few LD50 values have been deter- mined for marine organisms. Polikarpov (1966) lists LD50 values for 50 species of aquatic organisms, but the majority of these are freshwater organisms. White and Angelovic (1967) provided some LD50 values for several marine spe- cies irradiated with a 60Co source. For six species of marine adult fish, the LD50/30 (lethal dose for 50 percent mortality in 30 days) ranged from 1,050 R to 5,550 R, similar to values for freshwater fishes. White and Angelovic (1965, 1966) point to the need to describe radiation tolerances in terms of time curves for mean lethal dose rather than in terms of the usual LD5O,30. Figures 1 and 2 show the time curves for mean lethal dose for 14 marine fishes and invertebrates. Figure 2 shows, for example, that for the first 25 days, the oyster Crassostrea virginica is much more resistant to radiation than the clam Mercenaria mercenaria; after 80 days, however, the LD50 for the clam was greater than for the oyster. LD50 curves are needed, especially for the dominant eco- nomically important marine species in different ecosystems. However, because the levels of radiation required to kill ma- rine organisms are so high, actual kills by radiation in the environment are extremely unlikely. These experimental LD50 curves will, however, keep in proper perspective our view of the likelihood of mortality in marine organisms from acute radiation. CHRONIC EXPOSURE External Radiation Donaldson and Bonham (1964, 1966) have taken advantage of the migratory habit and the fecundity of chinook salmon, Oncorhynchus tshawystcha, to make a continuing long-term study of the effect on a population of chronic low-level ir- radiation from a 60Co source during embryonic develop- ment. Eggs were first irradiated at 0.5 R/day from shortly 2 5 01 & .1 .s T8 3 • • Paralichthys 1ethostigma o • lagodon rhomboides • • Eucinostomus sp o • Micropogon undulatus Mu1)11 cephalus Fundulus heteroclitus 20 40 Time After Irradiation (Days) 60 FIGURE 1 Mean lethal dose time curves for several species of marine vertebrates showing the dose-time combination at which 5O percent of the experimental animals died. (Reprinted with permission from White and Angelovic, 1966.) 3! i§ 200 in lo(1 140 120 100 so , 40 20 0 N,;. o • Mercenaria mercenaria • • Crassostrea virginica o • Arbacia punctulata • • Nassarius obsoletus A , Urosalpinx cinerea (99) • • Urosalpinx cinerea (d d) v • Uca pugnax . Falaemonetes pugio ^QL 40 60 80 Time After Irradiation (Days) 100 FIGURE 2 Mean lethal dose time curves for several species of marine invertebrates showing the dose-time combinations at which 50 percent of the experimental animals died. (Reprinted with per- mission from White and Angelovic, 1966.)

226 Radioactivity in the Marine Environment after fertilization until feeding commenced. The total dose was 33-40 R. The fingerlings were reared and then allowed to migrate to sea. Those that returned to the hatchery dur- ing the second year were precocious males; during the third and fourth years following irradiation, both male and female adults returned. Various crosses were made, some of which were reirradiated at 1.3 R/day to a total dose of 95 R. The initial dose chosen was about 40 times the calculated maxi- mum dose that the germ cells and young salmon could re- ceive in the Columbia River before migration to the sea. The radiation level used in the experiment was appreciable, amounting to 103 times the normal background, or 0.02 mR/hr. These series of long-term experiments involving large numbers of organisms (96,000 to 256,000 fingerlings were released per experiment) indicate that irradiation at 0.5 R/ day from the fertilization stage to the feeding stage pro- duced no damage to the stock sufficient to reduce the re- productive capability over a period of slightly more than one generation. Although abnormalities in young fish were increased by irradiation, the number of adults returning was not affected. On the contrary, the irradiated stock returned in greater numbers and produced a greater total of viable eggs than the control stock. Brown and Templeton (1964) and Templeton (1966) report on a series of experiments in which the eggs of plaice, P. platessa, were irradiated with a 137Cs source. Total doses ranging from 0.6 to 500 R were used, at rates of 10 mR/hr to 1 R/hr from fertilization until hatching. No significant differences at hatching were observed in the survival or in the number of abnormal larvae produced. Engel (1967) reports on studies of the effects of chronic low-level irradiation on the growth and survival of young blue crabs (Callinectes spidus). Single acute exposures had indicated that the sensitivity of these crabs is similar to that observed for other marine invertebrates. In the chronic irra- diation experiment, the crabs were irradiated at an average of 22.5 hr/day at rates of 3.2, 7.3, or 29.0 rads/hr. The total radiation doses received over 70 days were 5,105, 11,502 and 45,693 rads. A significant number of deaths due to ra- diation occurred only among the crabs that received the highest radiation dose. The death rate of the crabs that re- ceived 3.2 and 7.3 rads/hr was similar to that of the controls. All irradiated and control crabs molted at least once. The numbers of second and third molts were affected by the ra- diation dose. The crabs that were irradiated at 29.0 rads/hr molted least, and none had three successful molts. Crabs that received 3.2 and 7.3 rads/hr underwent more second and third molts than did the controls, although this differ- ence was not significant. Radionuclides in the medium do not constitute the only radiation source to which pelagic organisms are exposed in the environment. A high degree of sorption of radionuclides into or onto the egg, for example, could give rise to a radi- ation dose within, or in the immediate vicinity of, the de- veloping embryo that would be greater than that arising from the medium alone (Polikarpov and Ivanov, 1961, 1962; V. M. Brown, 1962; Brown and Templeton, 1964; Polikarpov, 1966). In addition, radiation from radionuclides incorporated into the developing tissues of an embryo may also be more effective in causing damage than external radi- ation alone (Polikarpov, 1966). Hibiya and Yagi (1956) and Mikami et al. (1956), using fallout ash and rainwater residues from weapons tests, re- ported on the effects of these materials on the development of fish eggs. Concentrations in excess of 2 X 10~9 Ci/liter were found to be lethal, and abnormalities and delay in hatching were observed in concentrations down to 4 X10~10 Ci/liter. The interpretation of these data must remain doubt- ful, however, since the radionuclide concentrations and chemical compositions of the ash and residues were not determined. Polikarpov and Ivanov (1961, 1962), Ivanov (1965), and Polikarpov (1966) reported on the effect of 90Sr-90Y at low concentrations in seawater on the development of eggs of Black Sea fishes. Polikarpov and his co-workers, who pio- neered the studies in this field, have reported on extensive studies with eggs of a large number of marine and freshwater species over the concentration range 10~14 to 10'* Ci/liter of 90Sr-90Y. Reduced hatching of the larvae and early mor- tality were seen at concentrations of 10~7 Ci/liter and above, and the number of abnormalities increased significantly and with remarkable consistency at concentrations of 10~10 Ci/ liter and above (Figure 3). V. M. Brown (1962), Brown and Templeton (1964), and Templeton (1966) conducted similar experiments using eggs of the brown trout (Salmo truttd) and of plaice (Pleuro- nectes platessa), maintained from immediately after fertili- zation until hatching in water contaminated with 90Sr-90Y over the concentration range 10~10 Ci/liter to 10'* Ci/liter. They did not observe any significant increase in mortality or in the production of abnormal larvae. Fedorov et al. (1964) reported that the eggs of plaice from the Barents Sea were sensitive to low concentrations of 90Sr-90Y in seawater. White and Angelovic (1966) report on the effects of chronic exposure to low levels of 137Cs on the developing eggs and larvae of mummichogs (Fundulus heteroclitus). The concen- trations of 137Cs used, 3X10-7, 3XlO^.and 3X10-5 Ci/ liter, produced no visible abnormalities. On the fourth day after fertilization, however, a general retardation in the rate of development was evident for those subjected to the high- est concentration levels. On the nineteenth day after fertili- zation (approximately 50 percent hatch), the groups in the highest and the lowest concentrations had a slight reduction in the number of fish hatching, but this difference was no longer observable by the time hatching was completed. Neustroev and Podymakhin (1966a), in similar studies with the eggs of the Atlantic salmon, Salmo salar, found

Radiation Effects 227 100 ~ 0) §- II £ .5 I! < ^ 80 60 40 20 10•10 10'6 10'14 10 Strontium.90 Concentration (Ci/1iler) that at 10-10 Ci/liter 90Sr-90Y, the rate of development of the egg was the same as the control up to the stage of one- third development of the yolk sac. Subsequently, the rate of development in the contaminated aquaria was more rapid than in the control. However, the mortality and number of deformities did not differ from those of the controls. At 10~8 and 10~6 Ci/liter, the rate of development was the same as that observed in the 10~10 Ci/liter experiment. Mor- tality and deformities were increased only at the higher level of radioactivity. Studies by Kulikov et al. (1966) of the effects of 90Sr- 90Y on the development of the eggs of the freshwater mol- lusc Limnaea stagnalis L. show that morphological abnor- malities, delay in development, and mortality were signifi- cant only at concentrations greater than 10~4 Ci/liter. Nelson (1968) studied the effects of radionuclides on Pacific oyster larvae, Crassostrea gigas. The larvae were reared for 48 hr following spawning in seawater containing either 65Zn, 51Cr, or 90Sr-90Y. The concentrations of each radionuclide range from 10~2 Ci/liter to 10~8 Ci/liter. Sig- nificant increases in abnormal larvae were detectable at the following minimal concentrations: 65Zn (carrier free), 1(H Ci/liter; 51Cr, 10•4 Ci/liter; 90Sr-90Y, KH Ci/liter. The effects of tritiated seawater on the germination of the asexually produced spores of Padina japonica have been studied. A reduced percentage of germination was observed in those subjected to a concentration of tritium of 3 X 10~2 Ci/liter. This concentration of tritium also had a marked ef- fect on the subsequent growth of the embryos, causing a decrease in the number and length of the rhizoids as well as in the number of cells in the multicellular filamentous thallus (Buggeln and Held, 1968). All of these studies have assessed radiation effects in terms of observable gross effects. Ivanov (1967) has con- sidered more sensitive parameters and reports on the effects of 90Sr-90Y in seawater on the mitotic activity and produc- tion of chromosome aberrations on the dividing cells of eggs FIGURE 3 Dependence of proportion of abnormal larvae of Black Sea Fishes on strontium-90 concentra- tion in surrounding seawater. (1) and (a) = abnormal mullet larvae; (2) and (b) = green wrasse (Labridae); (3) and (c) = horsemackerel; (4) and (d) = anchovies; (5) and (e) = from a mixture of pelagic eggs. (The figures denote the proportion of abnormalities in controls of the various species of fishes.) Left-hand graph without allowance for control, right-hand graph with allowance for control. (Reprinted with permission from Polikarpov, 1966.) of the Black Sea scorpionfish Scorpaena porans. As the con- centration increased from 10'10 Ci/liter to 10~5 Ci/liter, the mitotic activity of the cells decreased. At the same time, the percentage of chromosome aberrations increased, with sta- tistical significance when the concentration exceeded 10~9 Ci/liter. The types of aberrations were varied, with chromo- somal and chromatid bridges and fragments observed most frequently. At the highest concentrations, abnormal mitoses were observed. Experimental data concerning the radiation effects on developing embryos maintained under laboratory conditions in contaminated media are conflicting. In all these studies, the embryos were maintained under highly artificial condi- tions in the laboratory, including artificial fertilization. The developmental temperatures varied with species and experi- ments, ranging from 6°C to 24°C. In some experiments, antibiotics were used to reduce bacterial contamination. In addition, experimental incubation containers varied in ca- pacity from 60-ml petri dishes to 40-liter plastic containers, with experimental lots ranging from 30 to thousands of in- dividuals. The successful maintenance of marine eggs and embryos under controlled environmental conditions is yet to be developed for many marine organisms. In addition, more data are required on the effects of other environ- mental parameters before significant radiation effects can be demonstrated. Of particular significance in the work from the Soviet Union is the unique concentration effect response (Polikarpov, 1966). An increase in concentration of 90Sr- 90Y of six orders of magnitude (2 XI0-10 to 2 X10•4 Ci/ liter) no more than triples the abnormality production rate (Figure 3), and increases mortality only fivefold. If the ra- diation dose received by the developing eggs is proportional to the concentration and all other factors are equal, one would expect a more marked dose-effect response. The re- sults are inconsistent with the linear hypothesis of dose re- sponse as well as with data from many radiobiological and

228 Radioactivity in the Marine Environment TABLE 3 Mortality, Growth, and Radionuclide Concen- tration in Chinook Salmon, Oncorhynchus tshawytscha, Reared under Various Reactor Effluent Conditions, December 1965-April 1966" Treatment groups* (% effluent) % Mortality Mean Weig (5 mo) (g) Concentration nt (pCi/g wet weight) 24Na 51Cr 65Zn 0 18 0.70 77 19 6.8 2 10 0.82 750 38 20 4 13 1.05 1,390 S3 36 6 13 1.20 2,210 65 45 "After Olson (1967). ft At least 1,000 fish in each group. toxicological investigations. Although our knowledge of the dose-effect response at low levels of irradiation is limited, present knowledge suggests that perhaps factors other than radiation need to be considered and evaluated. The biological effects of the effluent from production reactors at the Hanford plant have been monitored for more than 20 years by rearing salmonids in diluted effluent. The three main factors in Hanford reactor effluent considered to have a potential effect are the thermal increment, radioac- tivity, and chemical toxicity, the last from the hexavalent chromium used as a corrosion inhibitor (Olson and Nakatani, 1965;Nakataniand Foster, 1966; Olson, 1967). Freshly fertilized eggs of salmonids have been incubated, and the fish reared in various concentrations of effluent until they reached migrant-sized fingerlings. The mortality, growth rate, and radionuclide concentration in chinook salmon reared under various effluent concentrations for 5 months during the 1965-1966 season are shown in Table 3. No significant lethality occurred in an effluent concentration of 6 percent, far above the existing levels in the river. The concentrations in the fish of the three gamma emitters, 24Na, siCr, and 65Zn, are approximately propor- tional to the effluent concentration. The body burdens at these levels have produced no demonstrable damage in chinook salmon. Internal Emitters The effects on rainbow trout, Salmo gairdneri, of ingestion of some biologically important radionuclides have been studied. Yearling trout were force-fed radionuclides in cap- sule form over extended periods to determine what quantity of radionuclides must be ingested to produce radiation syn- drome and damage. All of these experiments used very high levels of radionuclides, which would not normally be ex- perienced in a contaminated aquatic environment, as the controlled disposal of radionuclides is limited to lower levels by man's use of the environment. However, the data from these ingestion experiments help to keep observations of the body burdens of radioactivity in field-contaminated fish in proper perspective with respect to potential radiation dam- age in fish in general. In a series of feeding experiments, either 32P, 90Sr-90Y, or 65Zn was fed daily to rainbow trout at levels from 0.005 ^Ci/g/fish to high levels of about 10 juCi/g/fish (Watson et al., 1959; Nakatani and Foster, 1963; Nakatani, 1966). Table 4 summarizes the results. The hematopoietic tissues of trout were found to be the most radiosensitive, as in mammals. Leukopenia was an early indicator of radiation damage following the ingestion of beta-emitting 32P or 90Sr-90Y and gamma-emitting 65Zn. Depression of growth also indicated radiation damage for the rapidly growing yearling trout. The radiation syndrome, including leuko- penia, anorexia, loss of scales, lethargy, and growth depres- sion, was very pronounced for fish fed 32P at the higher levels and to a lesser extent for fish fed 90Sr-90Y. Because much of the energy from the gamma-emitting 65Zn is not absorbed, trout were able to ingest without observable ef- fect much higher levels of 65Zn than of 32P or 90Sr-90Y on a ^Ci/g/fish basis. In addition to the differences in the ra- diation characteristics of the isotopes, the rates at which the fish metabolize and the deposition sites for each radionu- clide also differ, although all three are "bone-seekers." Columbia River fish captured in the Hanford environs contain small amounts of virtually all of the radionuclides present in the water, but the only nuclides that accumulate in the fish flesh in significant amounts are 32P and 65Zn (Foster and Soldat, 1966). In 1965, the average concentra- tion in muscle tissue of whitefish, Prosopium williamsoni, was 200 pCi/g and 27 pCi/g for 32P and 65Zn, respectively. Substantial seasonal variations may occur, with a tenfold difference for 32P and a fourfold difference for 65Zn. In terms of radiation damage to fish, however, the concentra- tions are far below those levels for which demonstrable damage to fish can be expected. Laboratory trout with a body burden of 65Zn 10,000 times greater than that of river fish showed no detrimental effects. Similarly, trout with a body burden of 32P 100 times greater than that of river fish showed no effect, although leukopenia occurred if the body burden was 1,000 times greater. The determination of the actual dose absorbed by or- ganisms and tissues is fundamental to the assessment of the potential effects of radiation in aquatic studies. Such deter- minations have been reported in only a few studies, however. Although no dosimetric measurements were made for rainbow trout fed 65Zn, Erickson (1966) calculated the