CHAPTER 20 CHAPTER 20 Nuclear and Thermal
20.6 EFFECTS OF RADIATION ON TERRESTRIAL POPULATIONS
Reviews of responses of populations and communities of terrestrial plants47 and terrestrial animals48 to chronic irradiation have been published. In most contaminated areas, levels of radio- activity are too low to detect population- and community-level effects.2 Experimental field studies using 137Cs or 60Co as large sources of short-term and chronic gamma radiation have provided data on effects on natural communities of plants. For example, Woodwell’s studies49 with chronic gamma irradiation of an oak-pine forest demonstrated a relationship between plant physiognomy and radiosensitivity. Pine trees were the most sensitive, followed by shrubs and then herbaceous forms.
Low and crustose forms such as lichens were the most resistant. A reduction in species diversity was observed at 100 R/day (1 Gy/day).
The use of large gamma sources, such as those used to show changes in plant communities, is not a good method for demonstrating changes in animal populations and communities because many animals, such as invertebrates, are dependent on the presence of vegetation, which may be destroyed by the radiation. In addition, other animals, because of their natural mobility and shielding by vegetation or burrows, do not receive uniform doses.48 Moreover, radiation doses are difficult to estimate, as dose rate decreases as a power function with distance from the source. In the field, animals confined to enclosures have been irradiated chronically.2,48 In the laboratory, the acute response of animals is usually measured in terms of acute lethal doses, usually LD50(30) values, the dose lethal to 50% of organisms within 30 days; few laboratory studies involve chronic irradiation.
Many studies conducted in the area of nuclear facilities or testing have documented the uptake of radionuclides by natural biota. No appreciable radiation exposures to natural populations of terrestrial animals has occurred from normal operation of the reactors at nuclear power plant sites in the United States.18 Higher levels of radiation, either acute or chronic, are necessary to show effects on populations of plants and animals. However, information is available for several other contaminated terrestrial sites where estimated doses were calculated and effects on natural popula- tions studied. These sites include areas contaminated by reactor accidents, several national labora- tories, and waste sites. Where applicable, supporting evidence from relevant laboratory studies is included. The most highly radiation-contaminated terrestrial site is the area surrounding the Cher- nobyl nuclear reactor accident; these studies are noted here and reviewed in Chapter 24 by Eisler.
Effects of the Chernobyl accident on the flora and fauna in the surrounding contaminated area have been reviewed.50–53 Following the accident, the human population was evacuated from a highly contaminated area within a 30-km radius around the damaged reactor. Wildlife populations have become established in the absence of humans. This area, divided into a 10-km inner zone and an outer zone, now serves as a unique natural ecosystem of enormous radiological interest.53,54
Within three months of the Chernobyl accident, Russian scientists began studying the effects of radiation on plants and animals within the highly contaminated zones surrounding the plant and comparing the results with biota from reference areas. Because of the uneven distribution of radiation around the plant, doses to biota were often difficult to estimate. When studies were continued over a 3-year period, 1986 to 1989, recovery of the exposed populations took place, either by immigration of animals into the area or by a decrease in mortality and lethal genetic effects with time. Many of the studies address accumulation of genetic changes in the resident populations, the consequence of which are presently unknown.
20.6.1 Plant Populations and Communities
Of the flora in the area surrounding the damaged Chernobyl reactor, the pine and spruce (Pinus silvestris and Picae excelsa) in the nearby forest were the most radio-sensitive species, and by late summer of 1986, trees in a 4400-ha area were dead or dying. Doses to the trees were estimated at 80 to 100 Gy.50–53 Doses of 8 to 10 Gy killed younger trees and young shoots. Trees that received sublethal doses, 3 to 4 Gy, lost needles and developed morphological variations such as shortened and curved shoots. At the edge of the 30-km zone, where doses were estimated at 1 to 1.5 Gy, growth was temporarily suppressed. During 1987 to 1989, regenerative processes took over, and damaged trees formed gigantic needles. Mass flowering was observed. The deciduous forest, represented by birch (Betula tremula), aspen (Populus tremula), alder (Alnus glutinosa), and oak (Quercus robur), was more radioresistant, although foliage turned yellow and growth was tempo- rarily suppressed in the area that was sublethal to the pine forest. The deciduous species are considered ten times more radioresistant than pines.
Although no visible damage to herbaceous plants was reported in some studies, Savchenko reported increased phenotypic diversity and genetic modifications in several species, including Plantago lancelolata (Plantaginaceae) and Hieracium umbellatum (Compositae), found throughout
the contaminated area.53 Doses were not estimated. The following changes in plants were addition- ally reported in the contaminated area: an increase in chlorophyll mutation frequency, a decrease in seed viability, mass gall formation, and the appearance of leaf deformation/asymmetry and abnormal stem branching.
Two species were chosen for genetic toxicity studies. Chromosome aberrations were observed in root meristem cells of Crepis tectorum (Compositae), where gamma exposure rates ranged from 0.02 to 20 mR/hour.55 Beta exposure rates were estimated at ten times higher. For Arabidopsis thaliana (Cruciferae), there was a correlation between the radioactive contamination level, which ranged from 0.01 to 240 mR/hour, and frequency of plants with mutations,56 although there was no effect of these exposures on the germination rate of the plants.50
20.6.2 Invertebrate Populations and Communities
Species presence and population numbers of pine-forest-litter and soil fauna, such as mites, springtails, beetles, earthworms, and spiders within a 3-km radius of the Chernobyl reactor, were impacted by the fallout.57 Because of shielding by the soil, soil animals were affected to a lesser degree than pine-litter animals. Also, adult animals were less affected by 30-Gy doses (estimated by thermoluminescent dosimeters distributed on the soil surface) than were eggs and juveniles.
Among soil microfauna, first instar nymphs and larvae were absent in the soil following the accident; populations of young earthworms were decreased.50 The authors estimated that an absorbed dose of about 29 Gy devastated the soil microfauna, while a dose of about 8 Gy led to minor changes. In previously plowed soil, a surface dose of 4000 rad did not affect soil dwellers due to the shielding effect of the soil. Several specific studies were reviewed by Sokolov et al.50 The soil worm Aporectodea caliginose, a diploid species, suffered genetic damage in its male germ cells (chromosome fragments in 20% of the cells), and the population size was smaller in the contaminated zone than in a reference area. In contrast, the hexaploid parthenogenetic species Dendrobaena octaedra, which lives in the pine litter, had increased its population size over that of a reference area by 1988. The relative radioresistance of the latter species was attributed to the polyploid genome and the lack of predators.
Following the Chernobyl accident, changes involving greater phenotypic diversity and an increased frequency of rare phenotypes were observed in several species of dragonflies.53 Fruit flies (Drosophila melanogaster), which are known to be radioresistant, showed little difference in mutation frequency following the accident.58 However, in another study, an increase in dominant lethal mutations in fruit flies collected from an area with a radiation dose of 80.6 mR/hour compared with a reference area was reported.50
20.6.3 Small-Mammal Populations
Mammals are considered more radiosensitive than other taxonomic groups, with acute lethal doses ranging from 2 to 11 Gy.2 The mammal population in the Chernobyl area could not be compared pre- and postaccident, as the area was heavily inhabited by humans prior to the accident.50 But a 90% mortality of small mammals as a consequence of the accident was predicted, based on comparisons with reference plots and given the external radiation doses of up to 6000 R (approx- imately 60 Gy). By spring of 1987, the populations appeared to increase due to migration from adjacent noncontaminated areas50 and trapping of small mammals within the contaminated zone 8 years after the accident yielded greater success rates than in uncontaminated areas.59 Bank voles (Clethrienemys glareolus) captured in 1986 showed an increased number of corpora lutea but also an increase in embryonic mortality.50
An extensive study of genetic damage to small mammals at the Chernobyl site was carried out with the house mouse, Mus musculus.50,51,60 House mice were captured at three plots with average
external radiation doses of 0.1 to 1.5 mR/hour, 1 to 2 mR/hour, and 60 to 100 mR/hour (the latter approximately 0.6 to 1.0 mGy/hour). These animals did not show any signs of radiation sickness.
When males were mated with female laboratory mice, only two males (from the maximally contaminated area) of 122 were irreversibly sterile. For the rest of the males caught in this area, only temporary sterility was observed. In both males collected from this area and male progeny of pregnant laboratory female mice caged in the radioactive area, the frequency of chromosome aberrations as indicated by reciprocal translocations in spermatocytes was increased. The frequency of reciprocal translocations in spermatocytes increased linearly with increasing absorbed dose to the testes, which was estimated at 0.1 to 25 Gy for mice caught at the site.60
In 1994 and 1995, a study was undertaken to describe the diversity, distribution, and karyotypes of small mammals that live in the most radioactive sites within the exclusion zone near Chernobyl.59 An examination of karyotypes of 11 species of small mammals from the 30-km exclusion zone with species obtained from outside of the exclusion zone did not document gross chromosomal rearrangements. The diversity and abundance of small-mammal fauna was not reduced at the most radioactive sites, and the trapped specimens did not demonstrate aberrant gross morphological features other than enlargement of the spleen. The most commonly collected species were voles and shrews: Microtus arvalis, M. oeconomus, M. rossiaemeridionalis, and Sorex araneus. An examination of the mitochondrial cytochrome b gene of voles from Chernobyl did not reveal an increased mutation rate over that of voles from a reference area.61,62 In addition to enlargement of the spleen observed in some individuals collected at the site, physiological responses to radiation- induced stress may involve enlarged livers and thymus glands.63
Following the Chernobyl accident, several studies documented the genetic impact of radiation on small mammals. Bank voles (Clethrionomys glareolus) were extensively studied because they are common inhabitants of the area and have the highest levels of cesium and strontium. Through 1991, Goncharova and Ryabokon found elevated incidences of chromosome aberrations and poly- ploid cells in voles in the Chernobyl area.64 In Sweden, bank voles in a Chernobyl-contaminated area were found to have increased numbers of micronucleated polychromatic erythrocytes.65 How- ever, bank voles collected in 1997 from the most contaminated area at Chernobyl did not have increased frequencies of micronuclei66 and did not have reduced genetic variation.67 A possible explanation for these observations is the radioresistance or radioadaptation of bank voles.68,69 Bank voles trapped in the Chernobyl area and further irradiated with 60Co had increased life spans several generations after irradiation. The LD50/30 for this species is 966 R.70 Continuing monitoring studies of voles in the Chernobyl area will help to clarify the long-term genetic effects of radioactive contamination on natural populations.
Compared with Chernobyl, radioactive waste storage sites are minimally contaminated. Fol- lowing the partial draining of White Oak Lake, a settling basin for low-level radioactive wastes from the Oak Ridge National Laboratory, Dunaway and colleagues71–74 studied the rodent popula- tions utilizing the site. Doses to cotton rats (Sigmodon hispidus) were estimated by placing dosim- eters 1 m above ground level and subcutaneously within the animals. It was estimated that the rats were exposed to 0.004 Gy/week internally and 0.025 Gy/week externally based on free-air exposures of 15 mR/hr. The total dose was estimated at 0.03 Gy/week, and lifetime doses were probably less than 2 to 3 Gy. No effects on size, sex ratio, fertility, litter size, blood cell counts, or tissue lesions attributable to radiation were found. In the laboratory, an acute dose of 2 Gy resulted in no blood changes except a transient leucopenia in both cotton rats and rice rats (Oryzomys palustris).75 A dose of 6 Gy was lethal to rice rats but not to cotton rats. Chronic irradiation studies were not conducted with either species.
Since 1952, approximately 3 × 1017 Bq of solid radioactive waste has been buried at a 36-ha subsurface disposal site at the Idaho National Engineering Laboratory. Small mammals have burrowed into the site and dispersed some of the radioactivity.36,76 Radiation dosimeters implanted in deer mice (Peromyscus maniculatus) inhabiting the disposal area indicated radiation dose rates
of 0.004 to 418 mGy/day (median, 0.02 mGy/day); the dose at a reference site was 0.004 mGy/day.76 Comparisons with dosimeters placed 15 cm above the ground showed that the doses were primarily external from the buried waste and not from internal emitters (137Cs, 60Co, and 95Nb). The doses depended to a large degree on radioactivity in the area of capture and season, which in turn reflected animal movement outside the burrow. Implications of the dose were not assessed, but it was noted that the population density within the burial area was not significantly different from the density in an adjacent area. It is likely that the few animals that received the maximum dose rate of 418 mGy/day did not survive. Radiation dose rates received by Ord’s kangaroo rats (Dipodomys ordii) were much less than those received by deer mice. Doses to either species were less than those received by cotton and rice rats at the Oak Ridge site, where chronic exposure to 0.03 Gy/day did not result in significant effects on fertility.
A concurrent study concluded that radiation doses received by the deer mice inhabiting the area had no effect on body or organ weights and caused no increase in chromosomal aberrations.77 However, these observations were made two weeks after the mice were transported to an uncon- taminated site. Deer mice that were trapped near a radioactive leaching pond and that received dose rates of up to 0.01 Gy/day failed to exhibit any blood changes or pathologic lesions such as tumors.78 Using a shielded 137Cs radiation source to provide a uniform dose rate, French et al.44 exposed a population of pocket mice (Perognathus formosus) enclosed in a desert area to chronic yearly dose rates of 2.11 to 3.60 Gy/year (5.8 to 10 mGy/day). These dose rates were sufficient to increase the death rate of this species.
20.6.4 Avian Populations
The early literature on ionizing radiation and wild birds was reviewed by Mellinger and Schultz.79 Monitoring studies at radioactive sites did not reveal any apparent gross effects on birds.
Lethal doses (LD50/30) for various species are presented. Birds are only slightly less radiosensitive than mammals, with a range of acute lethal doses of 4.5 to 15 Gy.2
Ellegren et al. found an increased frequency of partial albinism among adult and nestling barn swallows (Hirundo rustica) captured close to Chernobyl compared to swallows captured in an uncontaminated reference area.80 As high as 15% of birds captured near Chernobyl in 1996 displayed partial albinism compared with < 2% in reference areas. Aberrant coloration, such as partial albinism, may be associated with increased risk of predation and reduced mating success;
this genotoxic effect appears to have resulted in a loss of fitness in the breeding population that may be associated with a significant decline in breeding population size between 1986 and 1996.
The authors proposed that the mutation was associated with germ cells and thus was heritable. The level of radiation in the area of capture at Chernobyl was 300 to 500 àR.
Bird populations were studied at the Idaho National Engineering Laboratory. Populations of barn swallows (H. rustica) that nested near the Test Reactor Area radioactive leaching ponds utilized leaching-pond arthropods as a food source and contaminated mud for nest construction.81 Adult birds contained primarily 51Cr (16.1 Bq/g), but 72% of the internal dose rate was due to 24Na (0.22 mGy/day). Thermoluminescent dosimeters placed in the nests indicated average external dose rates of 0.84 mGy/day for eggs and 2.20 mGy/day for nestlings, for a total of 54 mGy during the nesting period. Mortality rates for this population did not differ from that of a reference population. The mean growth rate of first-clutch swallows and mean asymptotic weights of immature birds were significantly different (p < 0.05) compared with the reference group, but they were within the normal range reported in the literature.
In a related laboratory-field study at the above site, freshly-hatched tree swallows (Tachycineta bicolor) acutely exposed to 0.9 Gy showed a normal growth rate, whereas those exposed to 2.7 or 4.5 Gy showed pronounced growth depression by the end of the nestling stage.82 Earlier, the authors had located a single tree-swallow nest with five eggs chronically exposed to 1.0 Gy/day throughout the nesting period. Fledglings from this nest showed severe growth depression.