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Paper RADIATION-INDUCED EFFECTS on PLANTS and ANIMALS: FINDINGS of the UNITED NATIONS CHERNOBYL FORUM

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Paper RADIATION-INDUCED EFFECTS on PLANTS and ANIMALS: FINDINGS of the UNITED NATIONS CHERNOBYL FORUM Paper RADIATION-INDUCED EFFECTS ON PLANTS AND ANIMALS: FINDINGS OF THE UNITED NATIONS CHERNOBYL FORUM Thomas G. Hinton,* Rudolph Alexakhin,† Mikhail Balonov,‡ Norman Gentner,§ Jolyn Hendry,‡ Boris Prister,** Per Strand,†† and Dennis Woodhead‡‡ INTRODUCTION Abstract—Several United Nations organizations sought to dis- pel the uncertainties and controversy that still exist concerning ALTHOUGH IT has been 20 y since the Chernobyl nuclear the effects of the Chernobyl accident. A Chernobyl Forum of international expertise was established to reach consensus on accident of 26 April 1986, controversy and uncertainty the environmental consequences and health effects attribut- still exist relative to the extent of death, damage, and able to radiation exposure arising from the accident. This long-term effects. To counter such confusion, the Inter- review is a synopsis of the subgroup that examined the national Atomic Energy Agency (IAEA), in cooperation radiological effects to nonhuman biota within the 30-km Exclusion Zone. The response of biota to Chernobyl irradia- with seven other United Nations’ organizations, estab- tion was a complex interaction among radiation dose, dose lished the Chernobyl Forum. The Forum’s mission was rate, temporal and spatial variation, varying radiation sensi- to reach consensus on the environmental consequences tivities of the different taxons, and indirect effects from other and health effects attributable to radiation exposure events. The radiation-induced effects to plants and animals arising from the accident, as well as to provide advice on within the 30-km Exclusion Zone around Chernobyl can be framed in three broad time periods relative to the accident: an environmental remediation, special health care programs, intense exposure period during the first 30 d following the and areas where further research is required. The other accident of 26 April 1986; a second phase that extended United Nations’ organizations involved were the Food through the first year of exposure during which time the and Agricultural Organization, the United Nations De- short-lived radionuclides decayed and longer-lived radionu- clides were transported to different components of the envi- velopment Program, United Nations Environment Pro- ronment by physical, chemical and biological processes; and gram, the United Nations Office for the Coordination of the third and continuing long-term phase of chronic exposure Humanitarian Affairs, the United Nations Scientific with dose rates <1% of the initial values. The doses accumu- Committee on the Effects of Atomic Radiation, the lated, and the observed effects on plants, soil invertebrates, terrestrial vertebrates and fish are summarized for each time World Health Organization, and the World Bank. period. Physiological and genetic effects on biota, as well as the In 2003–2004, two groups of experts from 12 indirect effects on wildlife of removing humans from the countries, including those most affected by the accident Chernobyl area, are placed in context of what was known (Belarus, Russia, and Ukraine), assembled as the Cher- about radioecological effects prior to the accident. Health Phys. 93(5):427–440; 2007 nobyl Forum to assess the accident’s environmental and human health consequences. A subgroup of the environ- Key words: National Council on Radiation Protection and Measurements; Chernobyl; health effects; accidents, nuclear mental section examined the radiological effects to non- human biota. This review presents their synopsis on the radiological effects to wildlife within the 30-km Exclu- sion Zone. It starts with a brief overview of what was * Savannah River Ecology Laboratory, University of Georgia, known about the radiological effects on biota prior to the Aiken, SC; † Russian Institute of Agricultural Radiology and Agroecol- ogy, Obnisk, Russia; ‡ International Atomic Energy Agency, Vienna, Chernobyl accident. Then the Chernobyl data are high- Austria; § United Nations Scientific Committee on Effects of Atomic lighted from three perspectives. First, general findings Radiation, Vienna, Austria; ** Ukrainian Institute of Agricultural Radi- ology, Kiev, Ukraine; †† International Union of Radioecology, Oslo, are presented as a function of three distinct time periods Norway; ‡‡ Centre for Environment, Fishery and Aquaculture, United in which very different radiological conditions domi- Kingdom. nated the post-accident environment. Second, general For correspondence contact: Thomas G. Hinton, Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, or email at findings of effects are presented from research on major [email protected]. classes of biota for which the most data exist (i.e., plants, (Manuscript accepted 29 June 2007) 0017-9078/07/0 soil invertebrates, terrestrial animals, fish). Third, the Copyright © 2007 Health Physics Society most recent and somewhat controversial cytogenetic data 427 428 Health Physics November 2007, Volume 93, Number 5 are summarized. An emphasis is placed on the impor- tance of secondary effects, such as adaptation, and the confounding indirect effects caused by human abandon- ment of the area. This comprehensive review is important because it encompasses the research of scientists from Belarus, Russia, and Ukraine, as well as many Western countries. The review forms a consensus of international expertise on the environmental radiological effects fol- lowing the world’s worst nuclear accident. Fig. 2. Range of short-term radiation doses (delivered over 5 to 60 d) that produced effects in various plant communities, rodents and soil invertebrates. Minor effects include chromosomal PRE-CHERNOBYL KNOWLEDGE OF damage, and changes in productivity, reproduction and physiol- RADIATION EFFECTS ON BIOTA ogy. Intermediate effects include changes in species composition and diversity through selective mortality. Severe effects (massive The biological effects of radiation on plants and mortality) begin at the upper range of intermediate effects animals have long been of interest to scientists; in fact, (Whicker and Fraley 1974; Whicker 1997). much of the information on human effects evolved from studies on plants and animals. Effects research paralleled Within the plant kingdom, trees are generally more the development of nuclear energy and concerns about sensitive than shrubs, which in turn are more sensitive the possible impacts of increased discharges of radionu- than herbaceous species. Primitive forms such as lichens, clides into the terrestrial and aquatic environments. After mosses, and liverworts are more resistant than vascular the mid-1970’s, sufficient information had accrued that plants. Radiation-resistant plants frequently have molec- several reviews summarized the effects of ionizing radi- ular and cellular characteristics that enhance their ability ation on plants and animals (Whicker and Fraley 1974; to tolerate radiation stress, and differences in plant- IAEA 1976, 1988, 1992; UNSCEAR 1996; Whicker community response can be explained, in part, by the 1997; Whicker and Hinton 1997). early work of Sparrow (1961). He showed that specific Some broad generalizations about effects from radi- nuclear characteristics are associated with high radiosen- ation exposure can be gleaned from the research that has sitivity in plants, but that sensitivity can be modified in been conducted over the last 100 y. Foremost are the time due to seasonal processes [e.g., dormancy, or the relatively large differences in doses required to cause onset of growth in spring (Table 1)]. lethality among various taxonomic groups (Fig. 1). Con- Scientific reviews (e.g., IAEA 1992) indicated that siderable variation in response occurs within a taxon due mammals are the most sensitive organisms and that to enhanced radiosensitivity of some species or life reproduction is a more sensitive endpoint than mortality. stages. Differences in radiosensitivities were also appar- For acute exposures of mammals, mortality generally ent when the doses required to transition from minor to occurs at doses Ͼ3 Gy while reproduction is affected at intermediate effects were documented for relatively short- doses Ͻ0.3 Gy. Chronic exposures alter the responses, term exposures. Data are summarized for various plant with mortality occurring at Ͼ0.1 Gy dϪ1 and reproduc- communities, soil invertebrates and rodents (Fig. 2). tion affected at Ͻ0.01 Gy dϪ1. Among aquatic organ- isms, fish are the most sensitive, with gametogenesis and Table 1. Nuclear characteristics and factors influencing the sen- sitivity of plants to radiation (Sparrow 1961; adapted from Whicker and Schultz 1982). Factors increasing sensitivity Factors decreasing sensitivity Large nucleus (high DNA content) Small nucleus (low DNA content) Much heterochromatin Little heterochromatin Large chromosomes Small chromosomes Acrocentric chromosomes Metacentric chromosomes Normal centromere Polycentric or diffuse centromere Uni-nucleated cells Multi-nucleated cells Low chromosome number High chromosome number Diploid or haploid High polypolid Fig. 1. Acute dose ranges that result in 100% mortality in various Sexual reproduction Asexual reproduction taxonomic groups. Humans are among the most sensitive mam- Long intermitotic time Short intermitotic time mals and, therefore, among the most sensitive organisms (Whicker Long dormant period Short or no dormant period Slow meiosis Fast meiosis and Schultz 1982). Radiation-induced effects on plants and animals ● T. G. HINTON ET AL. 429 embryo development being the more sensitive
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