EFFECTS OF RADIATION ON AQUATIC POPULATIONS

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CHAPTER 20 CHAPTER 20 Nuclear and Thermal

20.7 EFFECTS OF RADIATION ON AQUATIC POPULATIONS

Radionuclides have entered aquatic environments from natural sources, nuclear weapons testing, nuclear waste disposal, and accidental releases from nuclear power plants and via runoff from contaminated terrestrial environments. Associated with the presence of radioactive contaminants in aquatic systems is the potential for effects on aquatic biota. Exposure of such organisms may occur externally due to (1) radiation present in water and sediment and (2) the absorption of radionuclides onto the surface of biota, and internally as a consequence of absorption or ingestion.

As indicated in Table 20.2, annual doses received by marine and freshwater biota from natural sources of radiation are generally less than 5 mGy/year.20

Radiation-induced somatic and genetic effects have been observed in individual organisms fo llowing acute exposures in the laboratory.8,20,83–85 Several general conclusions have been drawn from acute and chronic laboratory investigations on aquatic organisms.8 Adult fish have radiation sensitivities similar to terrestrial mammals, provided sufficient time is allowed for temperature adjustments in the poikilothermic animals. Aquatic invertebrates tend to be more resistant to effects of radiation than vertebrates. Sensitivities of fish to radiation are dependent on the age of the fish and stage of embryological development. As pointed out by Blaylock and Witherspoon86 and the NCRP,8 such studies are often conducted at doses many times greater than that expected in aquatic environments associated with nuclear activities. Surveys of the literature indicate a lack of data on chronic exposures in the environment, especially at the population and community level of organization. 2,8,85

Included among the freshwater environments that have been studied for radiation effects are three U.S. Department of Energy sites: White Oak Lake at Oak Ridge National Laboratory, seepage basins and a reactor cooling reservoir at the Savannah River Plant, and ponds and streams at the Hanford Site; also studied are aquatic environments adjacent to the Chernobyl accident site and the Mayak plutonium reprocessing facility in Russia as well as marine atolls that have undergone nuclear testing activities. Each of these environments contains radionuclides at above-background concentra- tions. In some cases, effects have been noted in individual organisms; however, adverse effects have not been observed at the population or community level.8,20 For the most part, these studies have shown the resilience of populations of freshwater biota to doses of less than 10 mGy/day.

Field studies on the effects of radiation on the marine environment are primarily limited to those that have been conducted near Bikini and Eniwetok atolls and in the North Irish Sea. In both instances, contamination of the marine environment was associated with nuclear-weapons-related activities.

Long-term studies conducted in these areas have shown no impact on populations of aquatic biota.

Comparisons of freshwater and marine ecosystems indicate that radiation effects on marine systems may be less than those expected in freshwater systems based on the larger size of marine systems and therefore greater potential for contaminants to disperse, and on the greater number of species usually present in marine environments as compared to freshwater ecosystems.20 The studies dis- cussed below support the resilience of marine ecosystems to low-level ionizing radiation.

20.7.1 Plant Populations

The first large-scale introduction of radionuclides into the marine environment as a result of human activities occurred in 1946 on Bikini atoll. Both Bikini atoll and Eniwetok were used as the “Pacific Proving Ground” for test detonations of nuclear and thermonuclear devices. The biological studies that have been conducted in these areas have been summarized by Templeton et al.83 Intensive studies were conducted from 1950 through the 1960s to determine what effects radiation had on the marine environment. The studies concluded that, although individual organisms perished as a result of nuclear testing, the marine environment became repopulated with the impacted species over time. A few examples of effects on individual organisms from the area have

been found. Physiological functions of sessile algae were not noticeably altered one year after an explosion when algae were exposed to 5 to 20 to 30 mR/day.87 Abnormalities in plant growth have also been noted on Bikini and Eniwetok atolls. Chronic dose rates of gamma radiation of 0.13 to 0.37 Gy/day for 2 to 4 months (total dose 7.8 to 55 Gy) can result in abnormalities similar to those found on these atolls. Abnormalities in plant growth observed in the field at these sites include tumors and changes from vine growth to stalk growth in one plant.88

20.7.2 Invertebrate Populations

Located on the Oak Ridge National Laboratory’s Reservation is a 7-ha impounded embayment known as White Oak Lake, which has been used since 1943 as a settling basin for low-level radioactive waste and nonradioactive contaminants. contribute Most of the radioactivity within the lake is contributed by 137Cesium, 60Co, 90Sr, and 3H. Transuranic and 106Ruthenium tradionuclides are also present in the lake.89,90 Radioactivity within the lake water and sediment has varied over the years. Several species of fish, turtles, aquatic invertebrates, and plants have been reported in the eutrophic lake. Among them, chironomid larvae, snails, mosquitofish, and pond slider and snapping turtles have been studied for possible effects of chronic exposure to low-level radiation on the individuals and populations that reside in the lake. Although genetic effects and reproductive differences were observed between animals from the lake and animals from the reference sites as observed in the following discussions, adverse impacts at the population level were not expected to occur. Populations of aquatic organisms have been present since impoundment of the lake.

Larvae of the midge, Chironomus tentans, were collected from White Oak Lake on two separate occasions and examined for chromosome aberrations.91,92 Chironomids collected from the lake in 1960 received a daily dose of 6.24 mGy, approximately 1000 times normal background level.93 Comparisons of chromosomes within the salivary gland of these benthic aquatic invertebrates from White Oak Lake and reference populations indicated an increased number of chromosomal aberrati- ons in animals from the contaminated site. The frequency of endemic inversions was, however, similar between the areas. The author attributed the lack of difference to the possible elimination of inversion through natural selection or to genetic drift within the White Oak Lake populations.

In a follow-up study conducted 10 years later, when the dose rate received by chironomids was 0.3 mGy/day, no chromosomal aberrations were detected.94 A laboratory study with a related species, Chironomus riparius, revealed that 360 mGy/day was the lowest dose rate at which an increased frequency of chromosome aberrations could be detected in the larval and pupal stages of chironomids reared in tritiated water.95 A comparative study of chromosomal aberrations induced by chronic gamma radiation from an external 60Co source and beta radiation from incorporated tritium revealed similarities in the frequency of aberrations.96

Chromosomal abnormalities have also been measured in chironomids from the water reservoirs of the Chernobyl atomic power plant.53 In 1998, two years following the accident, all individuals of Chironomus balatonicus had chromosomal abnormalities, with 85.7% having heterozygous inversions, 85.7% with homozygous inversions, and 3.6% of the individuals with “B-chromosomes.”

The radiation dose to these organisms was not estimated.

A field experiment conducted in the early 1970s examined the effects of chronic irradiation on the population of an aquatic snail, Physa heterostropha.97 White Oak Lake snails, receiving a dose of 6.5 mGy/day, were found to have a significantly lower number of egg capsules per snail than did snails from the control population; however, snails from the contaminated site contained a significantly greater number of eggs per egg capsule. As a consequence, egg production was found to be similar in both populations. Laboratory populations of Physa heterostropha receiving a chronic dose of 10 mGy/hour (240 mGy/day) showed no significant differences from the control population in the number of egg capsules per snail, number of eggs per capsule, percent of eggs hatched, mortality, or snail size.98 A dose rate of 100 mGy/hour (2400 mGy/day), however, significantly decreased each of the population parameters.

Snails have been shown to be good biomonitors of radio-strontium in aquatic environments and to be relatively tolerant of elevated doses of radiation. Mollusks were collected from the Dnieper drainage area and throughout the Kiev administrative region following the Chernobyl nuclear accident.99 Radioactivity in shells and soft tissue were found to exceed pre-Chernobyl concentrations by factors as great as three orders of magnitude. The highest recorded concentrations were 4 to 5 MBq/kg in shells of Lymnaea and Plaorbarius. Abnormalities and impacts on snail populations were not recorded in the investigation. Gene frequencies at four polymorphic loci were examined in seven populations of the snail Dreissena polymorphs adjacent to the Chernobyl atomic power station.100 Recorded differences were attributed to conditions of the breeding site, such as substrate characteristics and water flow rate, and not to radiation or thermal differences.

20.7.3 Fish Populations

Studies have been conducted that examined the effects of chronic low-level radiation on mosquitofish (Gambusia affinis) populations in White Oak Lake.101,102 Fish collected from the lake in 1965 were found to have significantly larger brood sizes (when adjustments were made to correct for differences in maternal size) than did fish from the reference population. In addition, an increased number of dead and deformed embryos were noted in the White Oak Lake population. The fitness of White Oak Lake mosquitofish was further investigated in 1973 by the rearing of field-collected fish from the lake and from four reference sites.102 Significant differences were not found in the brood sizes of the F1 generations of the laboratory-reared fish from the five locations. It was therefore concluded that the larger brood size originally observed in White Oak Lake mosquitofish popula- tions was likely attributable to the eutrophic conditions of the lake and not to genetic adaptation as a response to radiation. The increased incidence of dead and deformed embryos did, however, persist in the White Oak Lake stock reared in the laboratory. Measurements of other characteristics revealed differences in the size and variability in the size of female fish and differences in the variability and mean critical thermal maximum of male mosquitofish from the White Oak Lake stock. Although these findings were used to support the explanation of the presence of radiation- induced recessive mutations in the gene pool of White Oak Lake, no significant negative impact on the overall fitness of mosquitofish from the lake was expected.102

As an added note, the dose rate to mosquitofish in White Oak Lake was 0.59 mGy/day in 1975 and 3.6 mGy/day in 1965. Both rates were considerably lower than the dose rate found to decrease brood size and increase sterility in the guppy, Poecilia reticulata, following chronic exposure in the laboratory.103 DNA strand breakage was also evaluated in mosquitofish (Gambusia affinis) from two sites associated with this facility.104 Fecundity was found to be negatively correlated with the amount of double-stranded breaks at one radioactively contaminated site. In addition, a higher proportion of strand breaks was found in females with broods containing deformed embryos than in females with normal broods. These data indicate a link between DNA strand breaks and potential population-level effects.

Fish from regions near Chernobyl have been examined for both genetic and morphological abnormalities. Chromosomal aberrations in the corneal epithelium were examined in carp from the cooling reservoir of the Chernobyl Atomic Power Station during 1987. The rate of mutagenesis between carp from the cooling pond and a site 60 km from Chernobyl were not interpreted as significantly different.50 DNA strand breaks and micronuclei were examined in channel catfish (Ictalurus punctatus) from the Chernobyl cooling pond and a fish hatchery 30 km from the Chernobyl site.105 Catfish from the cooling pond were found with a higher incidence of DNA damage; however, no difference in the number of micronuclei was detected. Radiocesium concen- trations in the cooling pond were at least 50% greater than at the U.S. Department of Energy Savannah River Site, where DNA damage was also detected in largemouth bass (Micropterus salmoides).106 The ability of catfish populations within the cooling ponds to withstand sediment exposures of up to approximately 3 Gy/day was attributed to possible acclimation and adaptation

over time.105 This may be supported by the lack of anomalous abnormalities in fish breeding near Chernobyl one year following the nuclear reactor accident.50

Activities of the Windscale reprocessing plant were responsible for the release of radionuclides into the marine environment as a consequence of the discharge of low-level radioactive effluent and a nuclear reactor accident in 1957. Fish in the North Irish Sea have been exposed to low-level radiation for over 20 years. Plaice (Pleuronectes platessa), a commercial fish species collected from the area in 1968 to 1970, showed no differences in average body length when compared to fish from other areas.20 In addition, laboratory studies conducted on plaice embryos revealed that a radiation dose rate of 0.05 mGy/day (measured in the area from 1967 to 1969)85 would not be sufficient to induce a discernible effect on individual plaice or on populations of the fish.107

Nuclear testing in the Pacific has also resulted in observable effects in marine fish. Thyroid tissue damage was observed in fish collected from Eniwetok for a period of 8 months following a nuclear detonation. The damage was attributed to the radiation from iodine, despite the absence of radioiodine from the fish thyroids.108

20.7.4 Turtle Populations

In the late 1980s, two species of turtles were collected from White Oak Lake and a reference site and examined for single-stranded DNA breaks, a nonspecific indicator of possible exposure to genotoxic agents in the environment.109 Both the pond slider (Trachemys scripta) and common snapping turtle (Chelydra serpentina) from the lake were found to contain a significantly greater amount of DNA damage than turtles from the reference site. Differences between species were not found. Turtles from White Oak Lake also contained significantly higher tissue concentrations of

137Cs, 90Sr, 60Co, and mercury. Because turtles in the lake were exposed to agents other than radiation that may have induced the DNA damage, radiation could not be singled out as the cause of the damage. The dose received by turtles in the lake was not determined, and comparative laboratory studies have not been conducted to ascertain whether radiation could induce the single-stranded DNA breaks observed in the field.

As with White Oak Lake, the Savannah River Plant is located on a U.S. Department of Energy facility. On the approximately 80,000 ha in South Carolina are five nuclear reactor facilities, two chemical separation plants, a heavy-water separating plant, small test-reactor facilities, and the Savannah River laboratory.110 Seepage basins on site have received radioactive and nonradioactive wastes from the plant in the past. A reactor cooling pond, designated Pond B, received fission products from a nuclear reactor between 1961 and 1964.111 A flow cytometric assay was utilized to assess the impact of low-level radiation on the DNA of turtles and ducks from contaminated aquatic environments on the Savannah River Plant. Bickham et al.112 collected slider turtles from two seepage basin complexes containing primarily 134Cs, 137Cs, 89Sr, 90Sr, and 3H. Chromium, mercury, and nitrate were also contaminants within the basins. Turtles from the seepage basins were found to possess significantly greater DNA content in red blood cells than turtles from the reference site. In addition, four turtles from the contaminated basins contained mosaic DNA. The enhanced amount of variation in DNA content was attributed to chromosomal rearrangements in the DNA, which can result in deletions and duplications of genetic material.

The presence of mosaic DNA is related to the proliferation of such cell lines. A correlation was found between the plastron length of the turtle, which is a rough estimate of age, and the amount of variation in cellular DNA. The dose rate to turtles was not determined, and the specific cause of the genetic damage in the Savannah River Plant turtles could not be ascertained. To determine whether low-level radiation could induce genetic damage as observed in the turtles from the seepage basins, slider turtles were collected from Pond B and cellular DNA content in red blood cells measured.113 As with the turtles from the seepage basins, a significantly greater variation in DNA content was found in turtles from the radioactive site than in turtles from the reference site. DNA from two of the turtles from Pond B showed evidence of aneuploid mosaicism. Although

the radiation dose received by the turtles was not determined, Pond B sliders were noted as containing average total body burdens of 137Cs and 90Sr of 842 Bq and 1879 Bq, respectively. Body burdens of the White Oak Lake pond sliders were, incidentally, within the range of that measured in the Savannah River turtles.114 Impacts of the variation in DNA content and presence of mosaicism on the turtle populations are unknown.

20.7.5 Waterfowl Populations

The same flow cytometric assay used on the Savannah River turtles was used to detect DNA abnormalities in ducks exposed to radionuclides in Pond B.111 Cesium-137 constituted 99% of the activity present in the reservoir. Game-farm-reared male mallards were released onto Pond B and allowed to roam free during the daylight hours for 12 months. Flow cytometric measurements were conducted on a regular basis by the extraction of blood from exposed and control mallards.

Differences were found between the Pond B mallards and the control groups’ only after the 137Cs concentration in the exposed ducks had reached steady-state equilibrium (mean of 2.52 Bq/g at 8 months). After 9 months, the coefficient of variation in DNA content was significantly greater in the Pond B mallards, with aneuploid mosaicism detected in 2 of the 14 pond ducks. Again, the impacts of these findings on the population level are unknown.

20.7.6 Aquatic Communities

The Hanford site near Richland, Washington, contains several aquatic systems with origins that date back to the Manhattan Project in 1943. Hanford ponds and streams were maintained to receive wastewater from nuclear reactor, reprocessing, and laboratory operations. The aquatic systems on site contain a variety of contaminants. Most contain radioactive waste in the form of mixed-fission and activation products with actinides including transuranics in some locations. Chemical waste was also released into some of the systems. In the mid-1970s, several of the aquatic ecosystems on site were studied to determine whether the presence of radioactive wastes could impact the community structure in terms of diversity and productivity.115 The study characterized limnological and radiological conditions in several ponds, ditches, and a trench. Although some differences in population parameters for algae, macrophytes, and invertebrates were found among the Hanford sites and between the Hanford sites and off-site systems, they could not be correlated with radio- logical differences. Comparisons of doses from ionizing radiation to aquatic biota in the Hanford ponds and streams to doses reported in the literature to cause minor to intermediate damage in aquatic organisms revealed that dose rates of 50 to 100 R/day in 100-N Trench may have been sufficient to induce limited damage to algae, invertebrates, and amphibians.

Aquatic environments were impacted by the Chernobyl atomic power plant (CAPP) accident in 1986. Many species formerly associated with the CAPP cooling ponds have returned to the ponds.51 A colony of beaver (Castor fiber) storks has returned to the ponds. Bivalve mollusk populations of Anodonata cygnea appear to be recovering and are actively growing following the radiation insult; however, populations of Dreissena continue to be depressed. Model estimates indicate an external radiation dose to aquatic biota of 2 to 3 mGy/day shortly after the accident.

Fish within these ponds also appeared to breed and grow successfully.

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