Phytoremediation of soil contaminated with low concentrations of radionuclides

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    l Department of Agronomy and Soils, Auburn University, Auburn, AL 36849-5412, USA; 2 USDA Forest Service, Pacific Northwest Research Station, 3200 Jefferson Way, Corvallis, OR 97331, USA; 3 Idaho National Engineering Laboratory, P.O. Box 1625, Idaho Falls ID 83415, USA; 4 College of Forest Resources, University of Washington, Seattle, WA 98195, USA; 5 Terrestrial Ecology Branch,

    US Environmental Protection Agency, Environmental Research Laboratory, 200 SW 35th Street, Corvallis, OR 97333, USA; 6 University of Georgia, Biogeochemical Division, Savannah River

    Ecology Laboratory, Drawer E, Aiken, SC 29802, USA

    (Received 28 July, 1994; accepted 5 March, 1995)

    Abstract. Ecosystems throughout the world have been contaminated with radionuclides by above- ground nuclear testing, nuclear reactor accidents and nuclear power generation. Radioisotopes char- acteristic of nuclear fission, such as 137Cs and 9Sr, that are released into the environment can become more concentrated as they move up the food chain often becoming human health hazards. Natural environmental processes will redistribute long lived radionuclides that are released into the envi- ronment among soil, plants and wildlife. Numerous studies have shown that 137Cs and 9Sr are not removed from the top 0.4 meters of soil even under high rainfall, and migration rate from the top few centimeters of soil is slow. The top 0.4 meters of the soil is where plant roots actively accumu- late elements. Since plants are known to take up and accumulate 137Cs and 9Sr, removal of these radionuclides from contaminated soils by plants could provide a reliable and economical method of remediation. One approach is to use fast growing plants inoculated with mycorrhizal fungi combined with soil organic amendments to maximize the plant accumulation and removal of radionuclides from contaminated soils, followed by harvest of above-ground portion of the plants. High temper-

    137 90 ature combustion would be used to oxidize plant material concentrating Cs and Sr in ash for disposal. When areas of land have been contaminated with radionuclides are large, using energy intensive engineering solutions to remediate huge volumes of soil is not feasible or economical. Plants are proposed as a viable and cost effective method to remove radionuclides from the soils that have been contaminated by nuclear testing and nuclear reactor accidents.

    1. Introduction

    Large areas of land have been contaminated by fission by-products resulting from nuclear bombs, (Mahara, 1993) above ground nuclear testing (Paasikallio, 1984; Eisenbud, 1987; Robison and Stone, 1992), the Chemobyl nuclear reactor accident (Clark and Smith, 1988) and nuclear reactor operations (Whicker et al., 1990; Nifontova et al., 1989). The atomic bomb dropped on Nagasaki in 1945 released large amounts of radioactive fission products. Most of the short life fission products have decayed in the last 50 years, but the long lived radionuclides such as 137Cs

    90 and Sr have persisted (Mahara, 1993). Contamination of soils with characteristic radionuclides, such as 137Cs and 9Sr has persisted for far longer than was originally expected (Kirk and Staunton, 1989).

    Water, Air, and Soil Pollution 88: 16%176, 1996. 1996 Kluwer Academic Publishers. Printed in the Netherlands.


    Radionuclides released into the environment are taken up by plants and redis- tributed throughout the ecosystem. Fission by products from these tests are present in soils and plants and represent an environmental threat to the health of local populations (Robison and Stone, 1992, 1989; Howard et al., 1991; Robison et al., 1988). A serious problem may arise when agroecosystems become contaminated. The annual dose from atmospheric releases results from inhalation, exposure to external sources and ingestion of contaminated food (Church et al., 1990). The annual dose from radionuclide releases to the average person is usually < 1% of that from normal background radiation (Gonzalez and Anderer, 1989). However the dose to each separate individual depends upon living and working location and diet (Whicker et al., 1990).

    Remediation of soil contaminated with low concentrations of radionuclides using present technology requires that soil be removed from the site and treated with various dispersing and chelating chemicals. Transporting soil requires heavy equipment, is time consuming and very costly; therefore, few attempts have been made to remediate areas that have soil contaminated with low concentrations of radionuclides. The time and cost it would take to remove soil contaminated with radionuclides from any one site, transport it to a treatment facility, treat it with dispersing and chelating agents and return the soil to the site, is problematic. In addition, the cost of disposing the vast amount of liquid dispersing and chelating chemicals which are then contaminated with radionuclides may be prohibitive. The Department of Energy Assistant Secretary for Environmental Restoration and Waste Management was quoted as stating that the $ 200 to 300 billion cost of radionuclide cleanup may be a dramatic underestimate (Watson et al., 1993).

    An additional negative factor to consider in site remediation is soil compaction by heavy equipment that is necessary to remove or transport soil. Compaction destroys many physical properties of the soil that have major impacts on chemical and microbiological processes which ultimately affect plant growth. Treating the soil with dispersing and chelating chemicals removes not only radionuclides but also soil nutrients. Soil nutrients are necessary for microbial as well as plant growth. Dispersing chemicals often adversely affect not only soil chemical processes, but also soil physical processes. After the soil is replaced, establishment of plants on a physically, chemically and microbiologically compromised soil is a formidable challenge.

    2. Plant Uptake of 137Cs and 9Sr from Soil

    A review of the literature indicates that a wide array of plant species occupying different habitats have been shown to accumulate large amounts of radionuclides from contaminated soils, and that the accumulation of radionuclides varies among plant species. Nifontova et al. (1989) found that plants accumulated between 530 and 1500 Bq of 137Cs between 300 and 1100 Bq of 9Sr in 12 forest and 5


    meadow plant communities in the vicinity of the Beloyarsk atomic power station in the Urals pine mountain region of Russia. Wallace and Romney (1972) found that a large number of plant species in the desert area near the Nevada Test Site accumulated substantial quantities of radionuclides in soils contaminated by above- ground nuclear testing.

    Trees have been shown to accumulate substantial quantities of radionuclides. Pinder et al. (1984) reported that Acer rubrum, Liquidambar stryaciflua and Lirio- dendron tulipifera accumulated significant quantities of 244Cm, 137Cs, 238pu, 226Ra and 9Sr. Robison and Stone (1992) found that Cocos nucifera accumulated sub- stantial amounts of 137Cs from soils contaminated by nuclear weapons testing on Bikini Atoll. They also reported that additions of potassium and phosphorus to the soil decreased the amount of 137Cs taken up by the trees. Entry et al. (1993) found that Pinus radiata seedlings accumulated more 137Cs and 9Sr than Pinus ponderosa. Entry and Emmingham (1995) found that potted Eucalyptus tereticor- nis seedlings removed 31.0% of the 137Cs and 11.3% of the 9Sr in sphagnum peat soil after one month of exposure.

    Accumulation of 137Cs and 9Sr in grasses and other herbaceous plants has also been widely documented. Dahlman et al. (1969) reported that Festuca arundinacea accumulated 42,143,00011.39 Bq of 137Cs per m 2 in 8 months. The total amount of 137Cs above-ground runoff and sediment from this area was less than 444,000 Bq of 137Cs. Salt et al. (1992) reported that Lolium perenne, Festuca rubra, Trifolium repens and Cerastium fontanum accumulated from 28 to 1040 Bq 137Cs g-1 of plant tissue in a re-seeded pasture in Scotland. Coughtery et al. (1989) found that a Festuca/Agrostis plant community in the United Kingdom accumulated 4-19% of the 137Cs deposited by Chernobyl fallout. Accumulation of 137Cs was higher in Carex spp. than 9 other species of grasses in an upland area in Great Britain (Coughtrey et al., 1989).

    Radionuclides are accumulated by phytoplankton and aquatic plants. Penntila et al. (1993) reported that these plants are consumed by aquatic and terrestrial animals and 137Cs and 9Sr have been known to bioaccumulate and eventually be incorporated into the human food chain. The ability to accumulate radionuclides also varies widely among aquatic plants. For example, Whicker et al. (1990) found that the aquatic macrophyte Hydrocotyle spp. accumulated more 137Cs and 9Sr than 15 other aquatic plants.


    The concentrations of radionuclides in plants are dependent on numerous environ- mental, physiological, and soil management factors (Breshears et al., 1992). The atomic configuration of Cs and Sr are similar to K and Ca, respectively; therefore, factors influencing movement, uptake and incorporation of these essential plant


    nutrients can be applied in a large degree to 137Cs and 9051". The availability of 137Cs to plants will depend on the type and amount of clay in the soil. 137Cs is selectively bound in the crystal lattice of smectitic clays, such as montmorillonite. Cation exchange capacity, base saturation and pH influence the behavior of 137Cs and 9Sr in the soil. The higher the cation exchange capacity of a soil the more 9Sr will be available for plant uptake. Base saturation is the amount of cations, other than H, A1 and Fe, adhering to the negative sites produced by the organic matter and clay in that soil. Therefore, the higher the base saturation, the more sites that are occupied by cations (i.e., mostly plant nutrients), and the less 137Cs and 9Sr will be taken up by plants. The amount of 9Sr taken up by plants is approximately reciprocal to the content of exchangeable base cations in the soil (Paasikallio, 1984). The amount of clay, soil pH and the amount of base cations especially potassium and calcium in the soil may limit the amount of 137Cs and 9Sr that plants accumulate from contaminated soils.

    The amount and type of organic matter in the soil will also have a significant influence on the availability of 137Cs and 9Sr in soil and subsequent plant uptake of these radionuclides. Paasikallo (1984) reported that more 137Cs and 9Sr was accumulated by Lolium multiflorum when grown in sphagnum peat than sand, silt or clay. Lolium multiflorium accumulated more 137Cs and 9Sr when grown on sphagnum peat than compost or Carex spp. peat. Essington and Nishita (1966) found that movement of 137Cs and 9Sr in soil columns complexed with chela- tors decreased when compared to uncomplexed 137Cs and 9Sr. In general, plants growing in soils containing high amounts of organic matter will accumulate higher amounts of radionuclides (Paasikallo, 1984).


    Fertilization practices also affect 137Cs and 9Sr accumulation by plants. Nitrogen fertilization in nitrogen-limited soils should have indirect positive effects on 137Cs and 9Sr uptake by increasing plant growth which will increase root growth and density, and ultimately increase the accumulation of radionuclides from the soil. Kirk and Staunton (1989) found that the higher the density of roots in the soil the more 137Cs was accumulated by plants. However, plant uptake of 137Cs may be substantially reduced by fertilization with large amounts of K or P, since K and Ca will compete with 137Cs and 9Sr for cation exchange sites (Robison and Stone, 1992).

    Water availability, also has a major effect on plant uptake of these radionuclides. Sazharova and Aleksakhin (1982) and Tensho et al. (1961) found that Hordeum vulgare, Medicago sativa, Oryza sativa and Zea mays accumulated substantially more fission products when they were irrigated. In seedlings of Pinus ponderosa, a native species of the western United States, extreme drought inhibited uptake of radioisotopes in solution, presumably because of reduced hydraulic conductivity


    (Vance, 1988). Conditions that maintain plant vigor and growth and reduce stress will enhance uptake of 137Cs and 9Sr. Plants adapted to growing conditions at the site contaminated with radionuclides should be evaluated at the site along with other plants that are known radionuclide accumulators. For example, P. radiata may remove radionuclides more efficiently in greenhouse conditions, but on a semi-arid site where P. ponderosa is native, the survival and growth of P.ponderosa may favor its potential to successfully accumulate and remove radionuclides from contaminated soil.


    Mycorrhizae are a symbiotic relationship between a soil fungus and host plant root. The plant provides the fungus with carbon in the form of sugars, and the fungus provides the plant with a mechanism that greatly enhances the ability of the root system to acquire soil elements and water. Mycorrhizal roots possess a consider- able advantage over nonmycorrhizal roots because the hyphal strands of the fungus ramify throughout the soil and exploit a greater soil volume than can roots alone. The extensive hyphae were first viewed as simple hyphal extensions of the absorb- ing surface. However, Nye and Tinker (1977) showed that the concentration of any immobile element in a soil will follow the laws of physics as it diffuses through the soil and is taken up by an absorbing surface. If its rate of absorption exceeds its diffusion rate, the concentration near the absorbing surface will decrease. The concentration of the element in the soil will continue to decrease until the ratio of uptake is equaled by the rate of replacement at the absorbing surface (root). A deficiency zone will soon develop around the absorbing surface. At this point, no physiological property of a living system can increase the rate of uptake because it is entirely limited by the element rate of diffusion through the soil.

    The rhizosphere, or zone immediately adjacent to the root, is an area of interface between roots, mycorrhizae and the soil. The rate of diffusion of a radionuclide along a gradient to the root can typically limit the amount of radionuclide taken up by plant roots in addition to restrictions that may be caused by the chemical form of the radionuclide. To increase...


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