The Effects of Atomic Radiation on Oceanography and Fisheries (1957)

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CHAPTER 10 EFFECTS OF RADIATION ON AQUATIC ORGANISMS LAUREN R. DONALDSON, Applied Fisheries Laboratory, University of Washington, Seattle, Washington and RICHARD F. FOSTER, Biology Operation, Hanford Laboratories, General Electric Company, Richland, Washington I. Somatic Effects of Ionizing Radiation THE EFFECTS of ionizing radiations on marine and fresh-water organisms have been studied by a few investigators since the early part of the century. The total volume of such work can by no means compare with that which has re- sulted from the intensive studies with more con- ventional laboratory animals. The value of much of the early work is impaired by inadequate or imperfect dosimetry. Nevertheless a sufficient block of information has been accumulated to permit several generalizations and at least some well-defined conclusions. A. Relative sensitivity of different organisms A broad review of the results obtained with the organisms of different phyla indicates that the lower or more primitive forms are generally more resistant to ionizing radiation than are the more complex vertebrate forms. Welander (un- published data) has summarized much of the data for which some approximation of dose can be made. Table 1 is a further condensation of these data which were obtained in experiments where whole body doses (usually X-rays) were administered. Owing to the great variety of circumstances under which the experiments were conducted, these data represent only orders of magnitude of effects. The algae and protozoa are most resistant with LD50 values in the order of many thou- sands of roentgens. The molluscs and crusta- ceans are somewhat more sensitive, with LD50 values of a few thousand roentgens (aquatic in- sects probably also fall in this category) and the fish are most sensitive with an LD50 of about one thousand roentgens —. in the same TABLE 1 RELATIVE SENSITIVITY OF DIFFERENT GROUPS OF ORGANISMS TO RADIATION (r) Dose which caused Group Algae .. 50% mortality 8,000-100,000 100% mortality 25,000- 600,000 Molluscs . Crustaceans Fish Insects l . 5,000- 20,000 500- 90,000 600- 3,000 10,000- 50,000 5,000- 80,000 370- 20,000 1 No data except for Culex and non-aquatic forms. "Latent" period 45 days Protozoa 10,000-300,000 18,000-1,250,000 45 min.-40 days 3 weeks-2 years 5 days-80 days 14-^60 days Investigators Bonham and Palumbo (1951); Crowther (1926) Bonham, et al. (1947). Ralston (1939); Back (1939); Back and Halberstaedter (1945); Halberstaedter and Back (1943); Powers and Shefner (1950); Feldman- Muhsam and Halberstaedter (1946). Bonham and Palumbo (1951). Bonham and Palumbo (1951). Corbella (1930) ; Welander et al. (1948); Foster et al. (1949); Ellinger (1939) (1940); Ssamokhvalova (1938); Sol- berg (1938). 96

Chapter 10 97 Radiation of Aquatic Organisms order of magnitude as that of other cold- blooded vertebrates. B. Relative sensitivity of different stages of development It must be recognized in any consideration of the relative sensitivity to radiation of different groups of organisms that considerable varia- bility exists between similar species. In com- paring the sensitivity of two species of snails, Bonham and Palumbo (1951) found that "at 10 kr, approximately one month elapsed before 50 per cent of the Radix died, while in the case of the Thais it was approximately one-half of a later stages of development. Unpublished work by Welander has shown the most radiation- sensitive period of silver salmon (Oncorhyn- chus kisutch) egg development to be a par- ticular stage during the mitosis of the single cell. For the most sensitive period an LD50 of only about 16 roentgens was observed. The change in sensitivity between different stages of development has also been shown with snails. Bonham and Palumbo (1951) showed that eggs of the fresh-water snail Radix japonica were more sensitive to radiation than the adults. Further studies of snails (Helisoma subcre- TABLE 2 RELATIVE SENSITIVITY OF DIFFERENT LIFE STAGES OF SALMONOIDS Stage irradiated Species Gametes * rainbow trout Eyed eggs chinook salmon Fingerlings chinook salmon Adult rainbow trout 1 In parent fish. year." Consideration must also be given to the different developmental stages of the same spe- cies. Since many investigators (Evans, 1936, Rugh, 1949) have correlated radiosensitivity with metabolic rate of the dividing cell, it is not surprising that dormant eggs of aquatic inverte- brates should be especially resistant. Bonham and Palumbo (1951) found that the two-week LD50 for dry Artemia eggs was about 50,000 roentgens, but after soaking the eggs for a short time in water, so that embryonic development was resumed, the radiosensitivity increased more than twofold. A review of the results of exposing salmo- noid gametes, eggs, fingerlings or adults to X-radiation supports the early concepts (Butler, 1936) that radiosensitivity decreases with age. Table 2 shows that the LD50 values range from 50-100 roentgens for gametes within the parent fish to about 1500 roentgens for adult trout. Welander (1954) studied in detail the effects of X-rays on different embryonic stages of rain- bow trout. His results with these aquatic forms confirmed the work of Russell and Russell (1954) and others working with mammals that certain critical periods exist during which the embryo is most sensitive to radiation. Table 3 shows some of Welander's data. Trout eggs were much more sensitive to ra- diation during the one-cell stage than during Approximate median effective dose (LDM) 50- 100 r 1000 r 1250-2500r 1500r Investigator Foster, et al. (1949) Welander, et al. (1948) Bonham, et al. (1948) Welander, et al. (1949) natum) eggs by Bonham (1955) showed that, in the one- and two-cell stages, resting eggs withstood from two to four times as much radia- tion as cells undergoing mitosis, and that later embryonic stages were less sensitive. C. Pathology of radiation damage 1. Different organs While effects of exposure to larger amounts of radiation than that sufficient to cause death of the organism have been studied by many investi- gators, few have studied in detail the physical and pathological syndromes of damaging but non-lethal exposures to radiation. Retardation in the rate of growth of snails ex- posed to radiation has been reported by Bon- TABLE 3 RELATIVE SENSITIVITY OF DIFFERENT EMBRYONIC STAGES OF TROUT TO X-1RRADIATION l Median effective does (I.IX) At end of yolk stage 57.8 r± 3.8* 313 r±12.4 461 r±15.9 454 r ± 19.4 415 r±22.0 904 r ± 38.5 Stage irradiated One-cell At hatching 78.3 r± 4.42 468 r ± 19.4 524 r±22.1 735 r ± 24.7 Thirty-two cell. . Early germ ring. . Late germ ring. . Early eye IrfUe eve 1 After Welander (1954).

98 Atomic Radiation and Oceanography and Fisheries ham and Palumbo (1951). Growth in length and weight of fish exposed to radiation is re- tarded as compared to control populations (We- lander et al., 1949). "The growth increment during the fastest growing period of the experiment was signifi- cantly less in a fish irradiated with 750 r or more of X-radiation and proved to be a very sensitive measurement of radiation damage and directly proportional to the amount of radiation given." The effects of X-radiation upon growth are not confined to the exposed population. Foster et al. (1949), reporting on the growth of rain- bow trout fingerlings produced from parent stock exposed to radiation prior to spawning, comment: "The rate of growth of the young during their first year of life was also found to be di- rectly affected by the amount of irradiation re- ceived by the parent fish. While variations in mortality became less with increasing age of the fish, variations in size became greater. Parents treated with 100 r produced progeny in which growth was slightly impeded, while parents treated with 500 or more r units produced progeny which grew appreciably more slowly than normal." Damage to specific organs and tissues of sal- monoid fish as a result of exposure to X-ra- diation has been studied by the staff of the Applied Fisheries Laboratory, University of Washington. Adult rainbow trout exposed to X-radiation prior to spawning were examined for gross ra- diation damage (Welander et al., 1949). The typical syndromes of radiation such as mass hemorrhage, petechiae and ecchymosis have been observed in all trout subjected to 1500 and 2500 roentgens. Gonadal hemorrhage was observed in fish exposed to 500 r of total body radiation. Exposures of 750 r resulted in hem- orrhagic areas in the peritoneum, while all ex- posures of 1000 r or more produced muscular hemorrhage. The eggs of rainbow trout exposed to radia- tion during early developmental stages (We- lander, 1954) produced fish showing retarded development. The eggs exposed during the 32- cell, late germ ring and early eyed stages tended to have a more juvenile appearance than the controls, viz., a larger eye and head in propor- tion to the size of the body. Other modifications evidenced in the young produced from radiated eggs were as follows: "The number of parr marks was significantly reduced in all stages after doses of 300 r or more, with doses as low as 25 r significantly altering the number in embryos irradiated dur- ing the 32-cell stage. "Reduction in number of dorsal and anal fin rays was general after irradiation of 32-cell, late germ ring and early eyed embryos. Doses from 75 to 100 r were significantly effective in re- ducing the fin ray number in these stages. "Gross superficial abnormalities observed in X-rayed trout were similar, though usually more numerous, to those found in the controls, with the exceptions of anomalies of dorsal and adi- pose fin produced by 200 and 400 r X-rays of 32-cell embryos." The eggs of chinook salmon (Oncorhynchus tshawytscha) exposed to X-radiation during the eyed stage with the results reported by We- lander et al. (1948), show somatic damage pro- portional to the amount of exposure. Histopathological studies on serial sections of the kidneys, with included hemopoietic tissue, the interrenal bodies, the spleen, the gonads and other organs of chinook salmon embryos and larvae revealed first the gonads, then the hemopoietic tissue as most radiosensitive. Exposure of the eyed eggs to 250 r greatly reduced the number of primordial germ cells in the gonads of the chinook salmon. This sharp reduction (Table 4) in number of cells at 250 r would indicate a measurable reduction at a much lower radiation exposure. The hemopoietic tissue of the anterior por- tion of the kidney of the chinook salmon pro- duced from eggs exposed to 250, 500 and 1000 r showed a reduction in number of cells and a temporary retardation in development, roughly proportional to the dose. Temporary cessation of mitosis at 1000 r and permanent cessation at higher radiations was noted. Counts of the glomeruli in the kidneys of young fish indicated a slight reduction in num- bers at 500 r with definite damage at exposures of 1000 r (Table 5). In general, it is observed that the tissues most sensitive to radiation damage are those in rapid division and growth. Gonadal and hemopoietic tissues that are in rapid division are many times more sensitive than those growing less rapidly. The very early embryonic stages of an organism

Chapter 10 99 Radiation of Aquatic Organisms TABLE 4 COUNTS OF THE PRIMORDIAL GERM CELLS IN THE GONADS OF CHINOOK SALMON COMPARED BY DAYS AFTER EXPOSURE AND BY DOSAGE l Days after Controls irradiation 9 or 33 250 r 42 500 r 25 1000 r 27 16 46 31 64 27 23 ... 32 3 108 ag 30 14 50 46 7 37 21 47 28 42 44 32 124 79 71 51 453 83 65 53 58 2 085 287 55 25 65 1,058 683 286 47 79 6,569 380 131 67 93 7 206 247 94 6) Average 1,595.4 182.6 89.2 43.1 1 Counts of over 1,000 r were arrived at by first making total counts on all five-micron sections and calculating the actual number of germ cells present us- ing the average size of the cell nucleus (9.2 microns) and actual cell counts of the other fish as a basis. In cases where every fifth section only was used (as in the 65th, 79th and 93rd day series) actual counts were obtained by multiplying original counts by five and then correcting for size of the cell nucleus. Data from Welander et al. (1948). are more radiation sensitive than the older, ma- ture forms. In all respects, the damage effects of radia- tion in fish are similar or identical to the ef- fects seen in other vertebrate animals. In gen- eral, the syndromes have a similar pattern throughout the animal kingdom depending on the dose. 2. Relative susceptibility of organs to ra- dioactive material For most experiments with aquatic organ- isms conducted to date radiation from external sources has been used. In the work of Chipman (1955) and Hiatt, Boroughs, Townsley, and Kau (1955) radiation from isotopic sources in the body was used, but at such low levels so- matic damage was not evident. The uptake of lethal levels of P22 is being studied by Watson (unpublished data). Adult rainbow trout chronically fed P22 died in ap- proximately 6 weeks when the concentration of the isotope in bone, the tissue of maximum up- take, reached a level of 18 to 65 ^c/g (giving a dose of about 1200 rads per day). Other trout remained alive during the 12 weeks' ex- periment with concentrations of P82 in the bone as high as 10 /nc/g. Although these fish showed no external evidence of radiation damage other than a slight reduction in growth rate, subse- quent dissection revealed that some damage had occurred. The syndrome was similar to that described for trout damaged by X-irradiation, especially the breakdown of the vascular system as evidenced by hemorrhage of the liver and musculature. In experiments that have taken place at Eni- wetok and Bikini Atolls the resulting radio- active materials that entered the water usually provided three types of exposure to the aquatic organisms: (1) some of the radiation came from contamination of the environment, (2) particulate matter, such as specks of radioactive debris often settled on organisms or adhered to mucus coverings, etc., or (3) the radioactive materials entered the organism through the food chain where it was absorbed and incorporated into the organism or eliminated by the usual biological processes. Although vast amounts of radiation may be present immediately following a weapons test, amounts that surely would produce measurable changes in the exposed aquatic forms, no spe- cific instances were found in which direct so- matic damage could be charged to radiation effects. It must be realized that in as complex an en- vironment as a coral atoll following the fate of individual populations is very difficult. The most sensitive forms, the fishes, undoubtedly are weakened from somatic and functional damage by radiation. Such weakened forms are usually eaten soon by the large carnivorous fishes that TABLE S COUNTS OF THE GLOMERULI IN THE KIDNEY OF CHINOOK SALMON LARVAE AFTER IRRADIATION IN EYED EGG STAGES'' Dose inr 23 30 37 44 51 58 65 79 93 Average 0 12 36 42 60 66 98 122 174 282 99.1 250 2 38 16 41 48 86 144 186 288 94.3 500 8 16 38 40 51 86 96 162 260 84.1 1000 . 0 26 28 25 46 2 70 64 120 42.3 1 After Welander et al. (1948), counts on 36 fish.

100 Atomic Radiation and Oceanography and Fisheries move into an affected area or, if not picked up at once following death, they decay so rapidly in the warm tropical waters as to be undetecta- ble in a few hours, thus escaping notice. II. Somatogenic Effects of Ionizing Radiation If we consider genetic effects in the strict sense of damage to chromosomes or genes, to the extent the modified characteristics are passed from one generation to the next, there is little to be found in the published literature describ- ing work on marine or fresh-water forms. Some effects on aquatic forms have been described, however, where gametes were exposed to radia- tion prior to zygote formation. The effects in such cases are due, at least in part, to somatic which died during the incubation period con- tained conspicuously abnormal embryos. The abnormalities could be attributed to deficiencies, improper differentiation of cell masses, dispro- portionate growth, or combinations of these fac- tors. Abnormal types of embryos occurred among the progeny of control parents and of parents which had received low doses of radia- tion which were almost identical with the types which occurred among the progeny of parents receiving large amounts of radiation. However, as the amount of radiation increased the relative abundance of malformed embryos increased and the degree of development attained decreased. Practically all of the embryos from parents treated with 1500 r and 2500 r were so ab- TABLE 6 EFFECT ON TROUT EGGS FROM IRRADIATING THE PARENT FISH 1 (Values are per cent of eggs which died at each stage) Stage of Development No embryo . . 0 18 5 50 32 2 100 23 0 500 244 750 42 6 1000 41 5 1500 68 1 2500 83 6 Blastoderm 08 0 3 3 2 5 9 06 3 2 2 9 4 5 Embryonic axis 4.3 46 43 8 2 21 1 29 5 22 1 11 5 Blastopore closed ... 10 4 4 3 7 236 22 5 15 5 5 5 0 3 Eyed 6.3 9 1 162 86 3 5 2 1 0 3 0 1 Hatching 8.7 11 4 10 1 14 5 6.3 63 09 o Total 39.6 62.0 60.5 85.2 96.6 1 Data from means (unpublished) of figure 1 from Foster et al. (1949). 98.1 99.8 100 damage but will be considered here because they represent some changes which may occur in off- spring of irradiated parents. The classical work of Henshaw and his col- leagues with the eggs and sperm of the sea urchin Arbacia demonstrated that X-radiation of the gametes delayed the first cleavage. Ef- fects of X-rays on gametes of fish have received some attention. In spite of massive doses of X-rays — 100,000 to 200,000 r — (Rugh and Clugston, 1955) to the eggs and sperm of Fundulus heteroclitus, fertilization can take place and some embryonic development is pos- sible although this may be parthenogenic from irradiated sperm. Solberg's (1936) work with Oryzias indicates that spermatozoa are three to four times as sensitive to radiation as ova, how- ever. Foster (1949) found that "The mean mortalities of the eggs obtained from parents subjected to 500 or more roentgen units were significantly greater than that of the eggs from the control parents. Most of the eggs normal that they died before closure of the blastopore. Irradiation of the parent fish thus increased the frequency of occurrence of malfor- mations." Table 6 illustrates that egg mortality was di- rectly related to the dose received by the parent fish and that the degree of development ob- tained by the embryo decreased at the higher exposure levels. Irradiation of gametes prior to "fertilization" is, of course, not the only means of producing abnormal embryos with ionizing radiation. We- lander (1954) found that abnormalities in- creased with dose among trout embryos irradi- ated at the 32-cell and early eyed stages. The production of phenocopies has been tentatively established. Welander, as stated earlier, found that trout irradiated with 200 and 400 r at the 32-cell stage had abnormal dorsal and adipose fins. Such anomalies arising from irradiation of cleavage stages would appear to result from a disturbance of the precursors.

Chapter 10 101 Radiation of Aquatic Organisms III. Other Considerations in Atomic Energy Use When potential effects of atomic energy in- stallations upon aquatic life are considered, ra- diation damage resulting from the release of radioactive isotopes is probably the primary con- sideration. Conventional types of pollutants must not be overlooked, however. Indeed, the chemical toxicity or high temperature of effluent released into a stream or lagoon could well be of greater concern than the radioactive materi- als. Olson and Foster (1955) have reported that very high concentrations of effluent from the Hanford reactors are toxic to young salmon and trout, not because of the radioactive iso- topes present, but because of the presence of dichromate. Krumholz (1954) states that: "The waste effluent which enters White Oak Creek consists of a heterogeneous mixture of chemical wastes resulting from laboratory, pilot- plant, and full-scale operations. Some of these wastes are radioactive and some are not." Since a variety of toxic substances is apt to be present in effluent from atomic energy plants, just as from other types of industry, care should be taken in appraising biological observations. If adverse effects on aquatic populations are ob- served, one should not immediately conclude that these are a result of radiation damage when, in fact, they may well result from altered chemical or temperature conditions. Serious radiation damage to aquatic popula- tions is certainly possible, however, under cat- astrophic or emergency conditions. It could also occur where there is continued release of inordinate amounts of isotopes which are con- centrated in the organisms. Such damage ap- pears unlikely, however, in situations where adequate radiation hazard control is extended to the environs of an atomic energy facility. Such control must go well beyond the sole considera- tion of maximum permissible concentrations for drinking water. Foster (1955) has pointed out that: "If radiophosphorus were allowed to reach the maximum level permitted for drinking water, organisms living in the water would suf- fer radiation damage and the fish would be un- safe for human food." If contamination in the fish and in other edible forms is to remain at a level which is safe for human beings, however, the radiation dose received by the organisms may not be intolerable to the organisms themselves. For example, the International Committee on Radiation Protec- tion recommends maximum permissible concen- trations (MFC) for P22 in drinking water of 2 x 10-4 (H.C P22 per cc, equivalent to an in- take of about 3 /*c P22 each week. If MFC's were based on a nominal consumption of one pound of fish per person each week, and an additional safety factor of 10 were applied ow- ing to the large populations involved, then the MFC for edible parts (flesh) of the fish would be 7 x 10-4 pC P22 per gram. This is only about one per cent of the concentration which Watson (unpublished data) found to be sub-lethal to trout in a 12-week period (although some ra- diation damage did occur). It seems unlikely, therefore, that significant damage would result to fish if the concentration of P22 in the flesh remained below 1Q-2 REFERENCES BACK, A. 1939. Sur un type de lesions pro- duites chez Paramaecium caudatum par les rayons X. Compt. Rend. Soc. Biol. 131 (22) =1103-1106. BACK, A., and L. HALBERSTAEDTER. 1945. In- fluence of biological factors on the form of roentgen-ray survival curves. Experi- ments on Paramecium caudatum. Am. J. Roentgenol. Radium Therapy 54:290-295. BONHAM, KELSHAW. 1955. Sensitivity to X-rays of the early cleavage stages of the snail Helisoma subcrenatum. Growth XIX:9-18. BONHAM, KELSHAW, and RALPH F. PALUMBO. 1951. Effects of X-rays on snails, crusta- cea, and algae. Growth XV: 155-188. BONHAM, KELSHAW, ALLYN H. SEYMOUR, LAUREN R. DONALDSON, and ARTHUR D. WELANDER. 1947. Lethal effect of X-rays on marine microplanton organisms. Sci- ence vol. 106, no. 2750. BUTLER, E. G. 1936. The effects of radium and X-rays on embryonic development. In, Biological Effects of Radiation, ed. B. M. Duggar, McGraw-Hill Book Co., Inc., N. Y., pp. 389-410. CHIPMAN, W. A. 1956. Passage of fission products through the skin of tuna. Fish

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