Effects on Populations of Exposure to Low Levels of Ionizing Radiation (1972)

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Chapter IV ENVIRONMENTAL TRANSPORT AND EFFECTS OF RADIONUCLIDES I. Introduction 22 II. Radionuclides in Air 22 A. Air Quality Assessment 22 B. Atmospheric Dispersion and Removal Processes 23 C. Natural Radionuclides 24 D. Land-based Nuclear Facilities 24 E. Marine-based Nuclear Facilities 24 F. Atmospheric Testing of Nuclear Devices 24 G. Underground Venting 24 H. SNAP Devices 25 III. Aquatic Systems 25 A. Natural Radioactivity 25 B. Acute Radiation Exposure 25 C. Chronic Radiation Exposure 25 D. Internal Emitters 26 E. Environmental Factors and Radiation Effects 26 F. Radiation Effects on Populations 26 IV. Soil-Plant Systems 27 A. Natural Radionuclides 27 B. Radioactive Fallout 27 C. Other Sources of Radiocontamination 28 D. Redistribution of Radionuclides 28 E. Radiation Effects in Soils 29 F. Radionuclide Entry into Plants and Radiation Effects 29 V. Animals and Animal Products 31 A. Relative Radiosensitivities 31 B. Routes of Exposure of Animal Populations 31 C. Animal Products as Sources of Human Exposure 32 1. Milk and Milk Products 32 2. Meat 33 3. Poultry 34 VI. Summary — An Ecological Approach 34 References 35 21

Chapter IV ENVIRONMENTAL TRANSPORT AND EFFECTS OF RADIONUCLIDES I. Introduction Previous considerations of radiation protec- tion have by and large ignored any possible effects of radiation on the environment - on organisms other than man. It has been assumed that at levels of radiation acceptable to man from past events there would be no observable biological effects on other individual organ- isms, and, furthermore, that there would be no effects on populations even if there were unde- tectable effects on individual organisms. Thus, the practice has been to limit monitoring and observation to those parts of the ecosystem close to man. It is well known, however, that various chemical pollutants have caused defi- nite effects on plant and animal life at ambient levels that have been traditionally and legally accepted by man. Therefore, our emphasis has been on the possible direct environmental ef- fects from radiation. Pertinent data on this subject have been reviewed in detail. With the development of nuclear energy, it is inevitable that the biosphere will be exposed to an increasing burden of radiation. For living species other than man, we need an estimate of the amounts and kinds of radiation that can be tolerated by the individual organism, the popu- lation, and the ecosystem without significantly changing the "balance of nature." The situa- tion is most complex because: (a) balance re- sponds to a multiplicity of natural and man- made factors of which radiation is but one; (b) knowledge is extremely limited on the response of ecosystems to small changes in the govern- ing factors; (c) interactions may be of great importance and practically nothing is known about them; (d) with a few notable exceptions, there are few data on radiation effects on var- ious species, especially on genetic effects. The same general types of radiation effects as described extensively for man in later chap- ters are expected in all living systems. Howev- er, radiation protection guidance for man rests on ethical consideration of the individual. For other living species the concern is not for the individual but for the population. Primarily for reasons of natural selection, it seems likely that genetic effects of radiation would be rela- tively unimportant and that effects on general mortality and fertility would be controlling. In addition to the problem of direct radiation effects on the environment, it is important to understand the transit of radioactivity in eco- systems wherever it occurs. This information is needed for several reasons: (a) to enable calcu- lation of concentrations of radioactivity that will reach man via biospheric pathways: (b) to permit mitigation of direct effects on human populations, especially following accidental events; (c) to indicate any particular species that might be exposed to unusually high levels; (d) to enable predictions of population expo- sures that might occur from given levels and patterns of contamination; (e) to serve as a basis for practical and effective monitoring systems. Information on transport relatable to testing of nuclear devices is dealt with only briefly because these matters have been cov- ered at great length in the scientific literature; more attention is given to situations that could arise from nuclear activities other than test- ing. II. Radionuclides in Air A. Air Quality Assessment Air is the transport medium which carries radionuclides released to the atmosphere from the sources as described in Chapter III to the 22

receptors of interest in the biosphere. A com- prehensive document in this area is "Meteorol- ogy and Atomic Energy" edited by D. H. Slade (1). The relationship of air quality to environ- mental impact requires an assessment of the amount and nature of radionuclides released, of air concentrations integrated over the time of interest, and of deposition or contamination patterns determined from atmospheric and geographical conditions (1-6). Mathematical simulation of concentration distributions has been more helpful generally than actual mea- surements of air quality because the require- ments of time and space sampling for the latter are difficult to fulfill adequately. Efforts at modeling have been reviewed in detail (7-10). In the future, more attention may need to be given to development and implementation of sam- pling procedures. Air quality measurements are normally re- quired to survey distribution of pollutants in anticipation of control strategies, to collect data for research purposes - environmental models, etc., or to document air quality condi- tions for public record (11). It is useful to have measurements of both air quality and meteo- rological parameters. These measurements can be used for radiation-dosage calculations (12). The mode of calculation depends upon whether the major effect is from the total radiation re- ceived from the cloud, instantaneous peak con- centrations or a combination of radiation dose from the passing of the cloud and from contam- inated surfaces following the passage. B. Atmospheric Dispersion and Removal Processes To understand the dispersion of radionu- clides in the atmosphere, two processes must be considered, transport and diffusion. From so- called "instantaneous" releases, such as explo- sions or short ventings the puff of material moves away from the source with a speed and direction determined by the wind at the moment of release (1, 5, 13-15). Surface air concentra- tions decrease with sampling time downwind of a source due largely to horizontal dispersion. For evaluating the impact of continuously emitting sources, relationships for periods of days are important. Reliable estimates of aver- age concentrations or exposures can be made from routine meteorological observations and appropriate diffusion equations (1, 5, 16-20). Understanding of factors governing global dispersion are limited although calculation techniques have been described (1,21, 22). Atmospheric concentrations of radionuclides can be corrected for radioactive decay by mul- tiplication factors that consist of the simple exponential term in the case of a single nuclide of known half-life or by appropriate power fac- tors for mixtures of radionuclides. Surf ace dry deposition can occur by gravita- tional settling (fallout), surface impaction, electrostatic attraction, adsorption, and chem- ical interaction. Two empirical approaches have been used to study this process. Deposi- tion velocities have been defined as the ratio of deposition rate to immediate ground level air concentration (23, 24). The other technique is to derive the deposition velocity from a material balance involving the mass flux of material through a vertical plane perpendicular to the mean wind direction. It appears that for parti- cles less than 10-15 micron diameter, the rela- tive effects of impaction, diffusion and adsorp- tion are more important; conversely, larger particles fall to the ground within rather short travel distances (25, 26). Removal of airborne radionuclides can occur by precipitation scavenging (1, 27), that is by rainout or snowout (in-cloud scavenging), or by washout (scavenging below the cloud by rain or snow). Radionuclides released from the ground will be transported by low level winds and diffused upward by turbulent eddies with removal primarily by washout at close-in dis- tances and by rainout at longer distances. Re- leases from high elevations (stratosphere) will be dispersed by the general circulation and tropospheric exchange processes will control subsequent removal. Washout by rain is gener- ally insignificant for particles smaller than about 1 micron diameter. Washout of reactive gases can be predicted by using the theory of molecular diffusion to water drops. Snow is apparently as effective as, to several times more effective than, rain at the same precipita- tion rate. Formal mathematical techniques for predicting precipitation scavenging are avail- able but must be used with caution. 23

C. Natural Radionuclides Most of the natural radioactivity in the at- mosphere is due to radon and its daughter prod- ucts, 218Po, 214Pb, 214Bi, and 214Po which be- come attached to submicron aerosols. Radon and its decay products have been most useful for studies of dispersion within the first 100 meters above ground and have shown promise as tracers of tropospheric transport on a hemi- spheric scale (28). Radon concentrations at ground level usual- ly range from 10 to 1000 picocuries per cubic meter for continental areas; the higher concen- trations (500-1000 pCi/M3) usually occur for periods of less than 24 hours as a result of stagnant weather conditions (29, 30, 31). High- er concentrations may also occur over areas exposed to uranium ore tailings or natural uranium outcroppings. Air concentrations over oceans may be lower than those over ground by two orders of magnitude. I). Land-based Nuclear Facilities Past studies of stack effluents from nuclear power and reprocessing plants have shown that almost all atmospheric releases are either gaseous or consist of particles less than 1 mi- cron diameter. These emissions are of the so- called elevated point source type and are treat- ed by the conventional Gaussian diffusion for- mulation. The stack emission is likely to in- crease rapidly during the dissolving of fuel and subsequently subside. Even low-level stack emissions will require consideration of average and atypical weather patterns for describing concentration distribution. E. Marine-based Nuclear Facilities There is a trend toward siting reactors along seacosts or large bodies of water. Quantitative information pertaining to movement of air- borne material over ocean and shoreline com- plexes, especially in regard to reactor siting, has been reviewed (13, 32, 33). Intuitively, one would expect atmospheric diffusion rates over extensive water surfaces to be less than for diffusion overland. Any assessment of atmos- pheric dispersion in coastal areas must consi- der the land-sea breeze phenomenon; informa- tion for individual sites is not usually availa- ble. Important factors include time of day, sea- son, comparative water and air temperatures, and local topography. The diffusion climate of each site must be studied individually. Nuclear power ships and submarines may represent a moving source with respect to po- tential radionuclide releases to the air. This makes any calculation of predictions very diffi- cult. F. Atmospheric Testing of Nuclear Devices The planning of nuclear tests and their safe execution require prediction and measurement of meteorological phenomena (22, 34, 35). The planning phase requires assessment of climato- logical data relevant to scheduling and moni- toring as well as forecasts of dispersion and deposition patterns for released radionuclides. The second phase requires meteorological and air quality measurements as well as dispersion- fallout forecasts made during and immediately after the test. For local fallout (within 100 miles) the most important information is accurate prediction of local wind, which can be gained from an ob- servation network including the use of weather radar. For distances beyond 100 miles, Fickian diffusion theory can be used. G. Underground Venting When nuclear devices are detonated under- ground in cratering applications, most of the radionuclides are attached to particulate mate- rial and rapidly settle to the ground; however, some of the material is either gaseous or of sufficiently small size to remain airborne. In contained applications, any venting usually is in the form of a small continuous leak of vola- tile radionuclides. The first step in assessment of venting is the determination of trajectories and various tech- niques are available including the central tend- ency method and kinematic methods (35). For cratering applications where the release is usually in the form of an instantaneous volume a specific dispersion model has been developed and usefully applied to a number of cratering tests. 24

H. SNAP (Systems for Nuclear Auxiliary Power) Devices These systems represent potential problems of high-altitude sources of radionuclides. Expe- rience from assessment of stratospheric dis- persion from weapons test fallout is most use- ful. The techniques and shortcomings of fore- casting dispersion in both the troposphere and stratosphere on a hemispheric or global scale have been well reviewed (21, 22, 36, 37). III. Aquatic Systems A detailed and comprehensive report entitled "Radioactivity in the Marine Environment" (RIME) (38) has recently been published by the Panel on Radioactivity in the Marine Environ- ment of the National Academy of Sciences. It deals with sources of radionuclides, distribu- tion, physical processes of water movement, chemical reactivity in seawater, sedimentary reactivity, radioecological interactions, distri- bution and effects of radionuclides in marine organisms, and implications for human radia- tion exposure. The present statement draws heavily upon the RIME report and emphasizes those considerations which need to be taken into account in protection of man and his envi- ronment through control of radiation. A. Natural Radioactivity Estimates for dose rates from total alpha activity to phytoplankton from the open sea ranged from 230 to 2800 mR/yr (39). Tissue dos- es in cod Gadus callarias and in haddock Gadus aeglefinus ranged from 8 to 27 mR/yr (40). The total dose rate to plaice, Pleuronectes platessa in the Irish Sea was estimated as 82 mR/yr with the seabed being the major source of radiation for this bottom-living species (38). I >. Acute Radiation Exposure Lethal response to acute radiation varies among organisms because of physiological differences; in the aquatic environment there are additional variables such as temperature, dissolved oxygen, chemical composition, and salinity. Some generalizations can be stated: (a) exclusive of the eggs and larvae of inverte- brates and fish, most of the aquatic organisms studied are relatively radioresistant; (b) mar- ine and freshwater species are similar in radia- tion resistance; (c) primitive forms are more resistant than complex vertebrates and older organisms more resistant than young. Bacte- ria and algae may tolerate thousands of roent- gens. The LDso for adult rainbow trout, Salmo gairdneri ranged from 300 to 3000 R, and for the most sensitive stage of the developing trout egg the LD50 was as low as 16 R (41). There are few data for marine species; estimates for six species of adult fish ranged from 1050 to 5550 R (42). It has been pointed out that radiation re- sponse is more meaningfully expressed in terms of a time curve rather than a simple LD50 be- cause various organisms have shown markedly different sensitivities as a function of time af- ter radiation exposure (43, 44). C. Chronic Radiation Exposure A series of long-term experiments with chi- nook salmon, Oncorhynchus tshawystcha, indi- cated that irradiation at 500 mR/day from the fertilization to feeding stage (total dose 33- 40R) did not reduce the reproductive capability over a period of slightly more than one genera- tion (45, 46). Abnormalities in young fish were increased, but the number of adults returning was not affected. Total doses of 0.6 to 500 R to the eggs of plaice, P. platessa from fertiliza- tion until hatching produced no significant effects in survival at hatching or in production of abnormal larvae (47, 48). Young blue crabs were exposed to 5105, 11502, or 45693 rads over a period of 70 days; deaths due to radiation occurred at the highest dose but not at the oth- ers (49). Experimental data on the radiation effects on eggs in contaminated media are conflicting, mainly, it is thought, because of difficulties in successful maintenance under controlled envi- ronmental conditions. Most of the work has been done using 90Sr and making observations of morphological abnormalities, delay in devel- opment, and mortality. Practically all workers have seen effects in the range of 10-4 Ci/liter whereas some have and some have not seen effects in the range of 10"4 to 10-10 Ci/liter (ref. 38, p. 226). Seawater containing a tritium con- centration of 3 x 10-2 Ci/liter was shown to af- fect the germination of spores of Padina japon- ica and the subsequent growth of the embryos 25

(50). The biological effects of effluent from pro- duction reactors at the Hanford plant have been monitored for more than 20 years by rear- ing salmonids in diluted effluent. No effects were observed at levels up to 6% effluent which is far above existing levels in the river (51-53). D. Internal Emitters Only 32P and 65Zn have been found to accu- mulate in significant amounts in fish flesh as a result of effluent from the Hanford plants (54). Studies were done in which varying levels of 32P, 65Zn and 90Sr were fed daily to rainbow trout for 17 to 25 weeks (55-57). Levels at which no effects were observed are as follows: -?2P - 0.006 Ci/g fish/day; 65Zn -1.0; 90Sr - 0.05; these levels are estimated to correspond to hundreds of rads total absorbed dose. Effects at higher levels included growth depression, mortality, and leukopenia. The term "concentration factor" is common- ly used to express the ratio of the concentra- tion of a radionuclide in an aquatic organism to that in its ambient water. Tables of concentra- tion factors are available for different radionu- clides, different trophic levels and different species, (ref. 38, p. 168). These data, although far from complete and adequate, may be help- ful for predictive purposes and any assess- ments should take them into account. But they must be used with caution because the values depend upon many variables. Phytoplankton and zooplankton may show concentration fac- tors in the order of 105 but values for other organisms are generally orders of magnitude. ? ]". Environmental Factors and Radiation Effects Because nuclear and desalination plants could release heat and highly saline water, there has been interest in the interaction of these factors on response to radiation. As a rule, greater radiosensitivity is observed fol- lowing temperature elevation during or after radiation exposure. Salinity also has an effect, which, however, cannot be simply generalized. It must be emphasized that any critical assess- ment should take into account to the extent possible the interactions of the environmental factors known to be important. These would include oxygen in addition to the above. F. Radiation Effects on Populations The major concern is with low-level radiation effects on populations and ecosystems in the aquatic environment rather than with effects on individuals. There are no data at the radia- tion levels of interest (levels associated with human population exposures of a few millerem per year); however, there are many high-level studies that do provide us with an important base-line. Controlled studies have been done on the effect of gamma radiation (25 to 75 R/hr for 19 hr/day) on Daphnia (58) and on the effect of repeated contamination with 32P and fi5Zn (~~ 7 - 30 /iCi/liter) on the reproductive capacity of mass cultures of Artemia which were followed for eight years (59, 60). Large-scale environ- mental observations are available from weap- ons testing at Bikini and Eniwitok at the Pacif- ic Proving Grounds (38, p. 232). Detailed stud- ies have been made in the Irish Sea costal area adjacent to the Windscale reprocessing plant where annual exposures of 7300 mrads could be accumulated by certain fish and at White Oak Creek and White Oak Lake (Oak Ridge, Tenn.) where larvae have been exposed to dose rates of about 240,000 mrads/yr for over 22 years (38, pp. 234-5). The major conclusion from all of these ob- servations is exemplified by the studies at the Pacific Proving Grounds. This aquatic environ- ment was exposed to intensely high radiation levels; despite initial large-scale destruction of life, the ecosystem was neither irreversibly nor irreparably damaged. After 25 years, life on the reefs has recovered and marine life has re-established itself. Individuals from unaf- fected areas have repopulated and occupied the reefs. Thus, if radionuclides are present in con- centrations acceptable for man, it is difficult to conceive that damaging effects on aquatic sys- tems could occur. Thought needs to be given to any possible effects on aquatic resources of changes in fe- cundity and mortality. A prevailing view, based on field observation, is that generally the normal survival of eggs is so low that large increases in the mortality at the egg stage would have very little effect on the mortality rate of the species (61). This would hold for all highly fecund species. It may be generalized that an accidental event involving large amounts of radioactivity 26

would be local in nature and there would be repopulation and recovery of the ecosystem with time. On the other hand, planned releases that could be more widespread would involve radioactivity at such low levels that any effect on fecundity or mortality of fish stocks could not alter the fish population as a food resource. The planned release would take into account distribution and reconcentration factors and the radioactivity allowed to enter this ecosys- tem would be regulated so that the use of fish for food would not expose the human popula- tion in excess of acceptable standards. IV. Soil - Plant Systems Depending upon chemical behavior, the soil can be a sink in which the individual radionu- clide may be stored with little chance of enter- ing the biosphere; or the soil may act as a re- servoir from which plants and organisms can be exposed for long time periods after the ini- tial soil contamination. Exposure can occur from direct uptake, entry into surface, ground, or irrigation waters, or direct irradiation. The role of soil is assessed mainly in terms of the amounts of various radionuclides that occur naturally or have been added to soil and knowl- edge of their behavior in the soil environment. A. Natural Radionuclides (62-80) Although numerous natural radionuclides are known to exist in soil, almost all of the ra- dioactivity is comprised of the following plus decay products: potassium -40, rubidium -87, thorium -232, uranium -235, uranium -238 (70). In addition, naturally occurring tritium and car- bon-14 are of interest because of their ready entry into living organisms. The total amount of natural radioactivity in one square meter of soil to normal cultivation depth (about 200 kg) is usually between 5 and 10 microcuries. Exceptional soils may contain more than three times the average concentration of potassium and rubidium and more than ten times the aver- age concentrations of thorium and uranium. Among the decay products of thorium -232 and uranium -238 are the gases radon -220 and radon -222, respectively, of which a small frac- tion escapes to the atmosphere where they de- cay to form radionuclides of polonium and lead which gradually return to the soil as a natural fallout (92). These do not contribute apprecia- bly to soil levels but do constitute a significant part of the plant content of lead 214, lead 212, lead 210, and polonium 210. B. Radioactive Fallout (81, 91) Radioactivity has been deposited upon the earth,s surface from nuclear explosions — nu- clear fission was predominant during the period 1958-60 and fusion during the period 1962-64. Soil levels of the long-lived fission products 90Sr and 13"Cs have been well documented in the United States. Average levels of 90Sr in soils increased from about 0.015 microcuries per square meter in 1958 to a maximum of 0.065 in 1967. The highest level found in the United States outside of the Nevada Test Site was 0.160 microcuries per square meter in a high rainfall area of western Washington (81, HASL 173). 137Cs deposition is about 50^ greater than that of 90Sr. Maximum accumulations of moderate-lived fission products occurred in 1559; soil levels of 144Ce, 106Ru, and 95Zr ranged from 0.40 to 0.74 microcuries per square meter (84) . In 1963, levels nearly as high were reached. There are no direct data on accumula- tions of short-lived nuclides in soil but esti- mates from milk levels indicate that deposits of 140Ba and 131I were about 1 microcurie per square meter in some areas of Utah in 1962. Soil levels of short-lived radionuclides are not contributors and have no relevance for human exposures via the food chain. Levels of carbon -14 and tritium added to soils from fallout can only be estimated indi- rectly from air and rainfall concentrations. Carbon occurs in soils mainly in humus and carbonate minerals and the 14C is added through incorporation of crop residues as fresh organic matter. However, this contribu- tion is small, has not been capable of measure- ment, and is estimated to be of the order of 0.014 microcuries per square meter (77). Hydro- gen occurs in soils in water and in humus. Based on rainfall analysis, tritium in wet soils may have reached 6 microcuries per square meter in 1963 (93). In peat soils, the humus could be a contributor of tritium but probably soil water is much more important. Rainfall concentrations indicate maximum accumulations of 0.04 microcuries of ;>4Mn and 27

0.2 microcuries of 00Fe per square meter in 1963 or 1964. C. Other Sources of Radiocontamination (94-101) Soil contamination can occur from reactor effluents, reprocessing wastes, mining opera- tions, and accidental releases. The pathway can be via the atmosphere, by irrigation or flooding of streams, or by seepage of contami- nated ground water from radioactive waste disposal areas. Experience from the reactor accident at Windscale, England, indicated that 131I con- tamination, which did not involve the soil, was most important; initial depositions were esti- mated to be about 40 microcuries per square meter for 131I and about 0.2 microcuries per square meter each of 89Sr, ™Sr, and i37Cs in the surrounding area (94). Data are available for levels of radionuclides in farm produce originating from irrigation water from the Columbia River below the Han- ford reactors. Following are the average con- centrations (pCi/liter) of the major radionu- clides in the water from 1958 to 1965: -^Na - 2000; 32? - 200; ^Cr - 5000; 65Zn - 200; ™As - 1000; 239Np - 2000 (102). Only 32p and 65Zn were found in the milk and these at average concen- trations of 700 and 500 pCi/liter respectively. The highest concentration of 32p was 5700 pCi/ liter in August 1964 following a period of unu- sually heavy irrigation. Patterns of ground water flow and radionu- clide movement in ground water have also been studied at Hanf ord. The ground water flow rate was about 1 mile per year requiring at least 15 years for movement from the Hanford disposal areas to the river. Most radionuclides moved only a few feet from the disposal site; only trit- ium, technetium -99, and ruthenium -106 were observed to move nearly as fast as the ground water (131). Redistribution of wastes from uranium min- ing depends greatly on local geography and climate. In some instances, the major method of redistribution has been by wind (103), in others by solution and transport of particles in streams (95). D. Redistribution of Radionuclides (104-14 ff) Radionuclides in or upon the soil can be redis- tributed or recycled by processes of erosion, sedimentation, desorption, leaching, and irri- gation. Redistribution through erosion and sedimen- tation may be very great in sloping areas, de- pending on average slope and amount of runoff. For example, more than half of the fallout 9°Sr on cultivated one-acre watersheds with from 10 to 15% slope had been eroded away in 1960 (133). Individual storm runoff has been shown to carry a few percent of fallout being deposit- ed in the current storm with radionuclide loss being roughly correlated with water runoff (134). Estimates of 9(>Sr movement from major river basins have been calculated from flow data and 90Sr concentrations in many locations (147). For the period 1958 to 1967, the amounts moved ranged from 0.1 to 10 mCi/km2 of drain- age area as compared with accumulated depos- its of 50 to 100 mCi/km2 in 1967. Thus, as a rough generalization, from 5 to 10 percent of the 9°Sr fallout was removed in areas with the greatest runoff (mountain and coastal regions), less than 5 percent in mid-sections of the coun- try, and less than 1% in arid sections. Deposition of sediment occurs in reservoirs and quiet stretches of streams, the extent de- pending upon particle size and holding times. It has been estimated that in the United States about one-fourth of the sediment produced is trapped in man-made reservoirs. Desorption of radionuclides from soils fol- lows the principles of ion exchange, the impor- tant factors being the properties of the radio- nuclide, the composition of the displacing solu- tion and the exchange capacity of the soil. Gen- erally, monovalent ions are most easily dis- placed, then divalent and trivalent ions. Anions are more easily displaced than cations because the charges on soil particles are predominantly negative. Downward movement in soils can occur by leaching or particle movement. Field studies in 1966 showed that 95% or more of the 9°Sr andi37Cs were in the top six inches of soil except where there had been mechanical move- ment of particles (81, HASL 183). Only tritium, technetium 99 and ruthenium 106 have been observed to move with ground water. Iodide also moves through soils that are low in organ- ic matter. 28

Irrigation may be an important process in the recycling of radionuclides from water to terrestrial food chains. In furrow irrigation, plants can become contaminated by uptake of radionuclides added to the soil; in sprinkler ir- rigation there is the additional direct contami- nation from the wetting of foliage. Limited experimentation leads to the generalization that sprinkler irrigation produces vegetation with about the same concentrations of 90Sr ar|d 137Cs as in the irrigation water (146). Long continued use of contaminated irrigation can result in the accumulation of long-lived radio- nuclides in the soil. Estimates have been made that the concentration of 9°Sr in a green crop on a fresh weight basis could reach 20 times the concentration in irrigation water after a few decades of irrigation. E. Radiation Effects in Soils (107-113, 148- 157) Gamma-emitting radionuclides spread on the soil surface irradiate rather uniformly any organisms living above the surface. However, the radiation dose decreases sharply with depth unless the radionuclides are mixed in the soil. For example, the gamma dose from fresh fission products on the soil surface would de- crease about 100 fold for each meter depth in the soil (156). Beta rays penetrate much short- er distances, being appreciably absorbed by a leaf or plant stem and almost completely by 5 mm of soil, depending upon their energy. Thus, the distribution of beta-emitting radionuclides on soil or plant surfaces is critical in determin- ing radiation exposure (153). Insects that feed or nest in leaf whorls or flower cups and some sensitive plant tissues such as actively grow- ing meristems may be exposed to much more beta radiation than would be expected from the general intensity of gamma radiation in the area. Alpha rays present little external radia- tion hazard to higher plants and animals; spe- cific hazards to single-celled organisms are largely unevaluated. Lower forms of life are generally more resist- ant to radiation than are the higher forms. For example, 10,000 rads would kill many higher plants or animals upon or within the soil which might release inorganic nutrients and stimu- late growth of fungi and bacteria. Doses great- er than 50,000 rads reduce the microbial popu- lation in soils and could result in selective kill- ing of different bacterial groups (157). Radia- tion doses less than 1000 rads would probably have negligible chemical, physical, or biologi- cal effects upon soils. The most sensitive chemi- cal effects appear to be increases in nitrate and ammonium concentrations in soil solution ob- served at exposures of about 1500 rads (148). From the standpoint of external irradiation, environmental releases of radioactivity con- trolled so that crops and animal produce would be acceptable to man are not at all likely to produce observable or significant long-term genetic changes in the organisms that reside in or on the soil. Any effects would require ex- treme contamination such as might result from close-in fallout from nuclear explosions or uti- lization of areas for high-level waste disposal. F. Radionuclide Entry into Plants and Ra- diation Effects (113, 158-172) Plants may become contaminated by absorp- tion through roots or through above-ground parts including leaves, stems and branches, flowers and fruit (113). Root absorption de- pends largely upon soil processes involving ionic form, pH, exchange capacity, moisture, and temperature. Some elements are strongly concentrated by plants (e.g. K, Rb, P, Na); some slightly concentrated (Ca, Sr, Mn, Zn); some not concentrated (Ba, Ra, Co); and some almost excluded (Cs, Fe, Ru, Sc, Y, Ce, Pb, U, Th, Pu) (154). Lowering pH values generally increases cation uptake and decreases anion uptake. In- creasing exchange capacity tends to decrease both cation and anion uptake. Highly organic soils permit increased Cs uptake as compared to mineral soils. Flooding of soils tends to in- crease the uptake of Cs and I. Legumes have a tendency to absorb more alkaline earths than alkali cations but the reverse is true for grass- es. Brazil nuts are effective accumulators of barium and rare earths with relatively high levels of alpha emitting nuclides. Direct contamination of foliage leads to a much higher radionuclide content than uptake through roots when the fallout rate is high. Three mechanisms of direct contamination have been recognized: foliar contamination which is retention and absorption through the 29

leaves; floral contamination, which is entrap- ment and absorption in inflorescends; and plant-base absorption, which is entry into the basal tissues of shoots or superficial roots by material initially lodged on them or washed down by rain from the foliage. Material is de- posited on plants by dust or other particulate matter, precipitation or sprays. Retention de- pends upon such factors as intensity and amount of precipitation, wind speed, particle size and density, wettability of leaves, leaf type and age, and thickness and continuity of the cuticle. To the extent that radionuclides are water-soluble, they may be absorbed through the leaves or basal tissues following much the same relationships described previously for root absorption. Once absorbed, processes of translocation influence distribution within the plant. Metabolites accumulate in certain plant parts depending upon the metabolism of the substance and the physiological stage of devel- opment. For example, calcium and strontium are found in cell wall materials and are not readily retranslocated to other parts. Elements such as potassium, phosphorus, sodium, rubi- dium and cesium are freely mobile. Phosphorus is accumulated in areas of high metabolic ac- tivity such as root tips, buds, flowers and devel- oping leaves. Carbohydrates are transferred from leaves, where they are manufactured, to areas of active growth and metabolism; this behavior would govern the distribution of con- taminating radioactive carbon compounds. In general, substances are preferentially translo- cated to the plant organ or part that is devel- oping at the particular time. This could be im- portant especially if contamination occurs simultaneously with development of a special- ized part that is utilized for food. Substances in plants are returned to soil by death and decay, leaching by rain or dew, exu- dation, and volatilization of gaseous sub- stances from plants. Much work has been done on radiocontami- nation of grazing lands because of the impor- tance of pasture as a route of exposure of man. Both direct contamination and absorption from the soil are important. Perhaps the pri- mary factor in soil uptake is the distribution of the nuclide in soil. Most pasture grasses obtain their nutrients from the top few inches of soil, and in humid regions have shallow root sys- tems; thus, the passage of time may remove contaminants from the rooting zone or other- wise reduce their accessibility. It appears that the rate of reduction of uptake of !)°Sr from soil is about 13-14% annually (197). The relative contribution of the soil t(0Sr to milk was report- ed in 1965 to vary from about 20 to 50% in dif- ferent years, being greatest in times of low fall- out and making only a minor contribution in years of relatively high fallout. In temperate regions, mineral soils, which bind 13?Cs, predominate. Studies have shown that only about 0.01% of i-^Cs artifically ap- plied to an average bluegrass pasture was transferred from soil to grass (105). Experience with organic soils in Florida indicated a gener- ally enhanced uptake from the soil in this re- gion (207). Although not a pasture plant, lichen is of considerable interest since, in arctic and su- barctic regions, it provides the main source of winter grazing for reindeer and caribou. Li- chen has no root system; all absorption occurs from its mycelial surface. The surface area of a typical lichen is about 10 times that of a typi- cal grass. Accumulation of deposited material is promoted by the long growth period (tens of years) and the fact that some nuclides can be translocated within the plant. The young green living top which is grazed can remain contami- nated for long time periods after contamina- tion because of translocation of nuclides from older parts. It is reported that up to 95% of deposited 1:*7Cs can be retained by lichen with a biological half-life in the plant of up to 17 years (106). There are little or no data on the effects of low level chronic irradiation of plants. Lilium and Tradescantia were affected by 30 to 40 R per day whereas plants such as gladiolus re- quired up to 9000 R per day before extensive damage was noted. Conifers such as pines and Taxus were affected at about 2 R per day (172). Chronic effects have been seen in oak trees exposed for 10 years at about 7 R per day (170). Generally speaking, flower parts and meris- tematic areas are much more sensitive to irra- diation than are leaves, stems, and roots. Plants with low chromosome numbers and small nuclear volumes are more radiosensi- tive than are plants with high chromosome numbers (including polyploids) and larger nu- clear volumes. In accordance with the general 30

pattern, it is difficult to conceive of significant harm to plant populations at radiation expo- sures that could occur under conditions which were acceptable to man. V. Animals and Animal Products It is difficult to quantify or define the effects of environmental radiocontamination upon animal populations in their natural habitats. The most useful approach seems to be to com- pare risks to animal populations with those to man in the same environmental situation; this we have attempted to do. In addition, we have summarized the present status with regard to assessment of radiation doses via milk, meat, and eggs, because these animal products are a primary route of transfer of environmental contaminants to man. A detailed review has recently been published that deals with the transfer of radioactive material from the ter- restrial environment to animals and man (173). A. Relative Radiosensitivities A scaleof relative lethal response of theadults of a wide variety of species can be constructed from the literature (174). Invertebrates are found to be more resistant than vertebrates with insects and mollusks, for example, being able to survive kilorad exposures. Among the vertebrates, mammals are somewhat more ra- diosensitive than birds, fish, amphibia, or rep- tile. Published values for the LD 50/30 of mammals following whole-body x- or gamma radiation range from about 150 rad (sheep, burro) to 1500 rad (desert mice) with that for man placed tentatively at 225-270 rad (175). Fewer data are available on the response of eggs, which are generally more sensitive than adults; however, it appears to be a reasonable assumption that relative susceptibilities among species can be ranked in the same order as that of adults. The conclusion can therefore be drawn that if exposed to the same acute ra- diation dose no animal species would be at very much greater risk than man. The primary concern in the context of peace- time environmental contamination is with ex- posures well below the lethal range and partic- ularly with continuous exposures at low rates. Under these conditions, the effects on animals are expected to be qualitatively similar to those on man as described in detail in later chapters; these include genetic effects and somatic effects comprised of malignant disease, cataracts, skin damage, non-specific aging, effects on growth and development, and im- paired fertility. It must be remembered that animals in their natural habitat do not usually attain more than a fraction of their potential lifespan, and under economic domestication are not usually retained beyond their reproductive lifespan. Thus, of all of the effects catalogued above, only impaired fertility may be of signifi- cance for the perpetuation of animal popula- tions. Both male and female germ cells of mammals are radiosensitive. On the basis of experiments with mice and dogs, observable effects on fertil- ity would not be expected at exposure rates less than tens of rads per year (176-178). However, Russian studies have reported sterility in young male tundra voles (Microtus oeconomus) trapped from areas where the uranium-radium content of the soil causes exposures up to 70 R per year (179). Thus, the application of existing population dose limits (0.17 rem average per year) across all animal populations would be expected to have an imperceptible impact upon them. B. Routes of Exposure of Animal Popula- tions Releases to the atmosphere probably have the widest potential consequences. External radiation from an airborne cloud and inhala- tion can present transient hazards but the main source of external exposure is likely to be materials deposited on or in soil. The whole- body radiation dose to animals living in close proximity to or burrowing in soil would be per- haps ten times greater than the average dose to man, especially from beta ray contributions. Inhalation and ingestion via drinking water are rarely major routes of entry of radiocon- taminants into the animal body. For a given contamination of air and water, it appears that animals are at no greater risk than man. The major route of exposure of contaminat- ing radionuclides for animals and man is through food. Under conditions of surface con- tamination of plant material relatively short- lived nuclides can be ingested in considerable 31

amounts depending largely upon the morphol- ogy of the foliage as described in the previous section. Uptake by roots from the soil presents a continuing source of contamination to plant- eating species. Ruminants are of particular importance; in their natural habitat, they either graze grass (sheep, cattle), or lichen (reindeer, caribou), or browse upon trees or shrubs (deer, some ante- lope, giraffe). They are most efficient as gather- ers of surface contamination. For example, it is estimated that a cow at pasture consumes daily airborne contaminant equivalent to that de- posited on 20 m2 of ground, as contrasted to a value of 10 cm2 for man representing daily con- sumption of green vegetables (173, 180). In ruminants, the unabsorbed ingesta constitutes an important source of internal exposure, par- ticularly to the female gonads. It is estimated that the whole body exposure from mixed fis- sion products ingested by a grazing cow from a nuclear detonation would approximate the ex- ternal exposure from material on the ground surface. Nevertheless, it can be demonstrated that the consumption of animal products by man is limiting to man rather than any hazard to the animal. It has been calculated that if cows were to consume 131I, 90Sr, and 137Cs at levels that would produce minimal pathological changes, the dose rate to children consuming fresh milk from them would be about 400 rem/ yr to the thyroid, 180 rem/yr to bone, and 170 rem/yr to the whole body respectively (113). During passage through a food chain, there can be progressive increases or decreases in concentration. Most elements decrease as they pass through the plant-herbivore-carnivore trophic levels. A few are concentrated, notably sodium in invertebrates and cesium in mam- mals. However, in mammals concentration fac- tors are relatively small. Ninefold increases in i37Cs have been reported through the plant- mule deer-cougar chain (181); fourfold increas- es in the lichen-caribou-wolf chain (182); and threefold increases in going from food to the human body (183, 188). Because man derives contaminating radionuclides from both plant and animal products, and because concentra- tion factors are relatively small, the concen- trations in mammalian predators would not be expected to differ from those in man by a large factor. C. Animal Products as Sources of Human Exposure Exposure of man from environmental radi- ocontamination arises mainly from contami- nated food, agricultural crops, and animal pro- duce. In the western world, milk has proven to be the primary vehicle. In addition, meat, poul- try, and eggs are a potential source. 1. Milk and Milk Products Most of the work on transfer of nuclides to milk has been confined to isotopes of iodine, strontium, and cesium. A frequently used para- meter is the "transfer coefficient" which is the percentage of the daily intake transferred to each liter of milk under steady-state condi- tions. Milk concentrations are also expressed in terms of concentrations in cut herbage or amount of nuclide per unit area of herbage. Use of area as a basis stems from the observation that the area from which a grazing cow ob- tains its daily intake is relatively more con- stant than the quantity of herbage consumed. In the case of strontium, the results are often expressed as "observed ratios" which denote the comparative behavior of strontium and calcium (184). Average transfer coefficients for isiI deter- mined for cows under laboratory conditions range from 0.5 to 1.0 percent of daily intake per liter of milk (113). Values from field trials have ranged from 0.12 to 2.4, the large variance aris- ing primarily from differences in physical prop- erties of fallout and in physiology of the ani- mals (185). Calculations have indicated that continuous grazing of cows on pasture carry- ing 1/iCi of 13il/m2 would lead to a milk con- centration of about 0.2 /LtCi/liter: a ratio of 5:1. (186). Field trials and also the experience of the Windscale accident have indicated that an average ratio of 10:1 would be more appropri- ate(187). Numerous studies have been done with 90Sr (113, 184). An average value of 0.08 has been determined under laboratory conditions for the transfer coefficient of 9°Sr to cow,s milk. Under field conditions, values from 0.05 to 0.22 have been reported. However, the transfer C03ffi- cient is dependent upon dietary calcium and it is more meaningful to express results in terms 32

of Sr/Ca ratios in diets and milk (OR milk/diet = 9°Sr/Ca in milk 4- 9°Sr/Ca in diet as measured at steady state). OR milk/diet values usually fall in the range of 0.08 to 0.16. Lower values have been reported in the literature but usual- ly can be shown to be in error because the 9°Sr/ Ca of diet did not reflect the total dietary in- take or because account was not taken of the contribution to milk from skeletal stores of strontium and calcium. A representative average value for the transfer coefficient of i3?Cs to cow,s milk is 1.2 but field values have been reported as low as 0.25 (113, 188). Low values are thought to be due to the binding of i3?Cs on clay particles associated with hay or by adsorption in the rumen contents (188). Data on transfer coeffi- cients for other elements are scarce but some ranges can be indicated (173): 1 to 4-Na, Zn, K; 0.1 to 1 - Ca, Fe, Co; 0.01 to 0.1 - Te, Ba, W, Po, Ra, U. The small amounts of very poorly ab- sorbed elements (e.g. i44Ce, 239pu) found in milk are thought to occur from fecal contamination (189). Limited studies have been done on the trans- fer of 131I, 90Sr, and i37Cs to milk products (190-192). From 0.4 to 2.7 percent of 131I in the original milk has been found per gram of skim milk, cream, butter, and cheese. In assessment of potential exposure from 131I in such prod- ucts, the time delay in consumption permitting radioactive decay must be taken in account. Relative concentrations of 9°Sr in butter, cot- tage cheese, and cheddar cheese following in vivo contamination of milk have been reported as 0.07, 6.8 and 0.34 respectively. Since the dis- tribution of strontium follows that of calcium in milk products there is nothing to be gained by substituting cheese for milk as a source of calcium in the human diet. For i3?Cs relative concentrations in butter vary from 0.03 to 0.11, in fresh cheese from 1.3 to 6.2, and cheddar cheese from 0.6 to 1.4. Considerable attention has been given to the prediction of milk levels following pasture con- tamination. The objectives are to help in plan- ning appropriate emergency measures follow- ing an uncontrolled release or to aid in the de- sign of installations that release radioactivity under controlled conditions. These models fall into three categories: (a) semiempirical, based on field observations of overall transfer (193- 197); (b) empirical, based on derived data for transfer from diet to milk, and assumptions as to amount of herbage grazed, proportion of deposited material retained on herbage, its rate of loss from herbage, and biological avail- ability (198-201); (c) sophisticated, attempting to take into account seasonal variations in feeding practices and pasture conditions (202). For accurate estimations, it is emphasized that there must be a field study at the time and place of contamination. Reliable models have been described for predicting the total intake of 131I and i3?Cs by an average individual from knowl- edge of the milk level at a known time after a contaminating event (203-206). 2. Meat The transfer of isil to muscle tissue in terms of percentage of daily intake per kilogram has been reported as 0.15 for the cow and 3 for the sheep. Values for i3?Cs are: cow-4; sheep-8; goat-20; swine-26. For 9°Sr, values of OR body/ diet range from 0.18 to 0.24 for the above spec- ies. Tissues other than muscle, such as liver and kidney, may tend to have higher levels of certain nuclides. Generally speaking, meat is not an important contributor of 131I and 90Sr to the human diet. Meat is estimated to contrib- ute from 30% to 40% of the i3?Cs in the aver- age U.S. diet. (See 113 and 173 for reviews of deposition in meat). In parts of Florida, a combination of high milk and beef levels of i3?Cs have led to body burdens in the human population 2 to 3 times higher than those reported elsewhere in the coterminous U.S. during the same time period (207, 208). Under some circumstances, meat from wild ruminants may have higher levels than from domestic stock. Mule deer from north-central Colorado which are primarily browsers, had i44Ce, i37Cs, 54Mn and i««Ru in their livers and a muscle concentration of i3?Cs 5 to 13 times that reported for beef and pork (209). In arctic and sub-arctic regions meat is a particularly important contributor to human dietary intake of radiocontamination. This is because of heavy surface contamination of slow growing lichen, dependence of grazing animals upon lichen for food in winter months, and high consumption of reindeer or caribou meat by the population. It has been estimated that animals feeding on lichen would have a 489-797 O - 72 - 4 33

daily intake of contaminating material 5 to 10 times higher than if they were feeding on green plants (210, 211). Although i3"Cs is the radio- nuclide contributing the largest radiation dose to these populations (estimated to reach an order of 200 mrad/yr) a number of others have also 'been detected in caribou flesh including 22Na, 40R, 54Mn, 55Fe, 60Co, 106RU, 11OmAg, 125Sb, 134CS, 210Pb, 210P0, and 228Th. 3. Poultry Poultry are generally reared under shelter and only relatively long-lived nuclides in stored feed are likely to present any problem. Howev- er, hens kept on free range could be a source of some short-lived radionuclides. For example, following the Windscale accident, eggs from such hens were judged next to milk as a poten- tial source of i3il, the activity per egg being about one-twentieth that per liter of milk (212). 137Cs is transferred effectively to eggs and muscle tissue whereas 90Sr is primarily seques- tered in the eggshell (213). VI. Summary — An Ecological Approach In general terms, man,s welfare depends upon the long-range quality of his total envi- ronment. Substances removed or added in large enough amounts can lead to imbalance or disor- der of a life support system that is the result of evolutionary development over the ages. With- in recent years, many thousands of waste prod- ucts from man,s agricultural, industrial, and domestic activities have been poured into the natural environment. There they may be stored, moved, accumulated, or dispersed, final- ly reaching equilibrium positions with effects apparent either at the time of contamination or much delayed depending on ecological behav- ior. These pollutants first were recognized to affect adversely man,s agricultural and in- dustrial base but within the past decade there has been increased sensitivity to direct effects on man himself. It is important to examine the release of ra- dioactivity to see if ecological considerations have been overlooked as for example in the case of DDT. For many years, DDT was judged to be under control by regulatory agencies, for its effects were evaluated primarily in terms of the target organisms. Many years were required before the movement of DDT in the environ- ment emerged to a point where it became of ecological concern. Radionuclides, just as nox- ious chemicals, can be stored, moved, and/or concentrated within various food chains and webs, with years and decades required before attainment of their ultimate distribution and expression of effects on sensitive organisms, including man. However, there are many reasons why the situation with regard to radioactivity differs from that of pesticides and other chemical pol- lutants. One set of reasons involves regulation and use: (a) release of radioactivity has always been under primarily governmental control or regulation; (b) the amounts released have been relatively small as by-products mainly of nu- clear testing, with no intent to produce effects on target organisms; (c) the possible hazards of radiation were recognized prior to environmen- tal radiocontamination and large research efforts have been under way since then, espe- cially on the biological effects of radiation and the details of food chains whereby radionu- clides reach the diet of man; and (d) regulation of possible population exposures was promul- gated in order to protect individual human beings. The other set of reasons involves bio- logical effects. Evidence to-date indicates that probably no other living organisms are very much more radiosensitive than man so that if man as an individual is protected, then other organisms as populations would be most un- likely to suffer harm. In fact, it is very difficult if not impossible to detect any effects of radio- nuclides in the environment even at concentra- tions much higher than the minimum estab- lished by regulation agencies. Therefore, the significant ecological aspect in regard to ra- dionuclides is to determine the pathways, rates, and concentrations as an essential measure of understanding their potential route to man through natural systems, which is quite differ- ent from the direct route of the traditional food chain e.g. grass-cow-man. With the increased use of nuclear energy by man, it is only prudent, despite the improbabili- ty of direct effects, that ecological considera- tions should be improved and strengthened. Where radioactivity is released to the bio- sphere, there should be programs adequate to answer the following: (a) how much, where, and 34

what type of radioactivity is released; (b) how are these materials moved through the environ- ment; (c) where are they concentrated in natu- ral systems; (d) how long might it take for them to move through these systems to a position of contact with man; (e) what is their effect on the environment itself; (f) how can this informa- tion be used as an early warning system to pre- vent potential problems from developing? REFERENCES (1) Slade, D. H. (Ed.), 1968: Meteorology and Atomic En- ergy, 1%-8: TID-24190, V. S. Atomic Energy Commission, Division of Technical Information (Available from Clearinghouse for Federal Scientific and Technical In- formation, Springfield, Virginia 22151). i (2) Pasquill, F., 1962: Atmospheric Diffusion, D. Van Nostrund Company, Ltd., London. (3) Scorer, R. S., 1968: Air Pollution, Pergamon Press, Inc., New York. (4) Smith, M. 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