phytoremediation of soil contaminated with low concentrations of radionuclides

P H Y T O R E M E D I A T I O N O F S O I L C O N T A M I N A T E D W I T H L O W

C O N C E N T R A T I O N S O F R A D I O N U C L I D E S

JAMES A. ENTRY 1 , NAN C. VANCE 2, MELINDA A. HAMILTON 3, DARLENE ZABOWSKI 4, LIDIA S. WATRUD 5 and DOMY C. ADRIANO 6

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 characteristic of nuclear fission, such as 137Cs and 9°Sr, 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 environment among soil, plants and wildlife. Numerous studies have shown that 137Cs and 9°Sr 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 accumulate elements. Since plants are known to take up and accumulate 137Cs and 9°Sr, 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 f rom

nuclear bombs , (Mahara, 1993) above ground nuclear testing (Paasikallio, 1984;

Eisenbud, 1987; Robison and Stone, 1992), the C h e m o b y l 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 radioact ive fission products. Most o f 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). Contaminat ion of soils with characteristic radionuclides, such as 137Cs and 9°Sr 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.

168 JAMES A. ENTRY ET AL.

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 9°Sr 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 9°Sr in 12 forest and 5

PHYTOREMEDIATION OF SOIL 169

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 9°Sr. Robison and Stone (1992) found that Cocos nucifera accumulated substantial 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 9°Sr 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 9°Sr in sphagnum peat soil after one month of exposure.

Accumulation of 137Cs and 9°Sr 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 9°Sr 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 9°Sr than 15 other aquatic plants.

2.1. INFLUENCE OF SOIL CONDITIONS ON PLANT UPTAKE OF 137Cs AND 9°Sr

The concentrations of radionuclides in plants are dependent on numerous environmental, 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 9°Sr in the soil. The higher the cation exchange capacity of a soil the more 9°Sr 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 9°Sr will be taken up by plants. The amount of 9°Sr 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 9°Sr 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 9°Sr in soil and subsequent plant uptake of these radionuclides. Paasikallo (1984) reported that more 137Cs and 9°Sr was accumulated by Lolium multiflorum when grown in sphagnum peat than sand, silt or clay. Lolium multiflorium accumulated more 137Cs and 9°Sr when grown on sphagnum peat than compost or Carex spp. peat. Essington and Nishita (1966) found that movement of 137Cs and 9°Sr in soil columns complexed with chelators decreased when compared to uncomplexed 137Cs and 9°Sr. In general, plants growing in soils containing high amounts of organic matter will accumulate higher amounts of radionuclides (Paasikallo, 1984).

2.2. INFLUENCE OF FERTILIZATION AND WATER AVAILABILITY ON PLANT UPTAKE OF 137Cs AND 9°Sr FROM SOIL

Fertilization practices also affect 137Cs and 9°Sr accumulation by plants. Nitrogen fertilization in nitrogen-limited soils should have indirect positive effects on 137Cs and 9°Sr 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 9°Sr 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 9°Sr. 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.

2.3. MYCORRHIZAL PLANTS AND UPTAKE OF 137Cs AND 9°Sr FROM 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 absorbing 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 radionuclide uptake by the plant, either the rhizosphere area must increase or the diffusion of the radionuclide to the rhizosphere must increase (Barber, 1984). Diffusion could be increased by increasing the gradient of the radionuclide concentration. Limitations to this process are related to the chemical form of the radionuclide. Chemical extractions of radionuclides from both the rhzosphere and the bulk soil could be used to determine the quantity of radionuclides in each chemical form and how each chemical form will change over time.

Hyphae of mycorrhizal fungi serve to exploit a wider volume of soil outside the element deficiency zone and translocate absorbed elements to the root (Harley and Smith, 1983). Sanders and Tinker (1971) showed that translocation of elements (especially immobile elements) in the hyphae of mycorrhizal fungi was great


enough to accommodate the rate of inflow. Hyphae of mycorrhizae also develop deficiency zones about themselves. However, the provision of a new absorbing surface by growth of the hyphae is much less expensive in carbon cost to the plant than growth of a root. Since 137Cs and 9°Sr have a low mobility and concentration in the soil solution (Fried and Grakoviskiy, 1988; Kirk and Staunton, 1989; Mahara, 1993), mycorrhizal infection of roots should greatly enhance the uptake of these radionuclides. In addition, elements such as 137Cs and 9°Sr have been found to be more readily absorbed by mycorrhizal than nonmycorrhizal plants. Appreciable quantities of elements accumulate in the hyphae of mycorrhizal fungi (Harley, 1989). In ectomycorrhizae, this accumulation is especially pronounced because the sheath (hartig net) acts as an organ which concentrates elements (Harley and Smith, 1983).

Inoculation with a specific mycorrhizal fungus could increase the ability of the plant to acquire necessary nutrients while removing large quantities of 137Cs and 9°Sr from contaminated soils (Rogers and Williams, 1986; Clint and Dighton, 1992; Entry et al., 1994). Not all mycorrhizal fungi will be equally effective, therefore specific associations should be tested for efficacy. Entry et a l . (1994) found that the species of fungus forming the ectomycorrhiza with a specific tree species can have significant effects on the amount of 9°Sr accumulated by that tree. Rogers and Williams (1986) found that inoculation of Melilotus officinalis and Sorghum sudanese with vesicular arbuscular mycorrhizae increased the amount of 137Cs accumulated from contaminated soils.

One problem with mycorrhizal inoculations is that the specific mycorrhizal fungus established on a plant root in the greenhouse will not necessarily be the mycorrhizal fungus on that root after a short time in the field (Harley and Smith, 1983). Most plant species will vary in their ability to establish mycorrhizae with fungi. Environmental, plant physiological and soil conditions will affect mycorrhizal specificity on most plants (Molina et al., 1992; Brand, 1992). The specific fungus that will form mycorrhizal relationships with a plant in the field cannot be controlled with any degree of accuracy. What can be more easily controlled is the percent of fine roots that have mycorrhizae. Establishment of mycorrhizal fungi on plant roots in a field environment can best be accomplished through plant growing conditions, fungal inoculation and manipulation of the type and amount soil organic materials.

3. Remediation of Radionuclide Contaminated Soils with Plants

Remediation of soils contaminated with radionuclides could be accomplished by using fast growing perennial plants combined with specific mycorrhizal fungi or other root associated microflora, to maximize plant's uptake and accumulation. There are numerous reports of plant accumulation of radionuclides, especially 137Cs and 9°Sr (Wallace and Romney, 1972; Pinder et al., 1984; Salt et al., 1992;

PHYTOREMEDIAT1ON OF SOIL 173

Coughtrey et al., 1989; Murphy and Johnson, 1993). An important objective would be to screen and find a series of plants that can quickly accumulate and remove radionuclides from contaminated soils. Entry and Watrud (unpublished data) found that switchgrass (Panicum virginatum) removed 36.2% of the 137Cs and 43.6% of the 9°Sr added to a sand growth medium after 5 monthly cuttings. Laboratory experiments indicate that certain plants may be able to remove radionuclides, especially 137Cs and 9°Sr from soil over a time period of 5 to 20 years. Plant dispersal of radionuclides from the site could be minimized through plant management, selection of plants that are less palatable to grazing animals and fencing.

Managers could periodically harvest the above-ground portion of plants. High temperature combustion would be used to oxidize plant material concentrating radionuclides in ash for disposal.

Physical and chemical properties of the soil could be altered by adding organic amendments, chelating agents and fertilizer, to enhance the availability of radionuclides to plants while decreasing the mobility of these radionuclides in soil.

The most desirable soil conditions would be those that enhance plant uptake of radionuclides while decreasing radionuclide mobility in the soil. Achieving this condition in soils may be approached in two ways: I) by improving the ability of the plant to take up radionuclides as through mycorrhizal associations or 2) by altering the chemical form of the radionuclide in the soil to increase its availability to plants. The second approach would require an addition to the soil of a chelator, such as diethylenetriamine-pentaacetic acid (DTPA), which would alter the radionuclide form so it is more available to the plant while still leaving it in a form that will not be leached from the soil. Organic matter will complex with 137Cs and 9°Sr to remove them from absorption sites on mineral solids while lowering soil pH and base saturation which also increase radionuclide availability to plants. Many naturally occurring soil organic compounds as well as synthetic chelators are bound by soil clays, oxides and mineral surfaces preventing their downward movement in the soil. Oxygen bonds, cation bridges and chelated metal bridges have been suggested as mechanisms to explain organic fixation (Wallace and Wallace, 1983). If oxygen bonds or other cations are providing bonding to clay sites, then chelated radionuclides would still be accessible to plant roots. Either natural or synthetic chelators could react with radionuclides, such as 137Cs and 9°St fixed to clay particles making these elements more accessible for plant uptake. Binding of these radionuclide-organic complexes to clay particles would prevent increased movement of these radionuclides through the soil while increasing the availability to uptake by plant roots.

3.1. SELECTION OF PLANTS FOR BIOREMEDIATION

One method for selecting plants to remove radionuclides from contaminated soils is to use a three stage approach. The first stage could be to survey and assess plants growing on a contaminated site to determine if these plants can accumulate sig-


nificant quantifies of radionuclides. The life cycle of plants needs to be considered because it could affect rates of radionuclide accumulation. Multiple assessments may be needed to account for differences in plant development. In the second stage, managers could screen plants by comparing plants growing on contaminated sites that have been found to accumulate significant quantities of radionuclides with fast growing plants that could grow on the site, and plants known to accumulate large amounts of ions related to the radionuclides, such as potassium or calcium. These plants would be screened for their ability to remove radionuclides from the contaminated soil in greenhouse or garden plots. The third stage would involve testing the effectiveness of plants selected from the first two stages to remove radionuclides from soil in combination with mycorrhizal inoculations and various soil organic and fertilizer amendments. This multi-staged procedure could be carried out most efficiently in time and cost by proceeding with several stages concurrently. Many parameters in this procedure are known. Botanists, soil scientists and agronomists have a good understanding of environmental conditions, organic amendments and fertilization regimes that favor maximum production for many fast growing plants. Perfecting methods to maintain the formation of mycorrhizal associations with a specific fungus or sets of fungi presents the greatest challenge. However, a practi- cal method for using plants to remove radionuclides from contaminated soils can be accomplished before the mycorrhizal inoculation method and the absolute best organic amendment for each soil is found.

3.2. ENVIRONMENTAL CONSEQUENCES

Site managers must recognize the environmental consequences of establishing non- native plants on a site. There are numerous examples of land managers introducing exotic plant species to solve a specific problem. The introduced plant may become an aggressive weed species replacing native species and costing millions of dollars to eradicate. Containment of seed and pollen dispersal may have to be considered also. This problem can be circumvented if the plant is harvested before flowering. Using plant species that are native to the site if preferable. Native plant species are adapted to the site climate and, therefore, to grow well under site conditions. If native plant species are numerous in the site area, more opportunities are afforded to find perennial and woody plants that are vigorous growers and good radionuclide accumulators. If the site is harsh and lacking plants, selectivity would be limited. Strategies for screening and selecting plants should be developed on a site by site basis.

4. Summary

Large areas of land have been contaminated with low concentrations of radionu- elides. Remediation using the present energy intensive engineering solutions are


not feasible or cost effective. The practice of removal and treatment of such huge volumes of soil is logistically difficult and cost prohibitive. Removal of low concentrations of radionuclides from soil using plant bioremediation could save time and prove to be less costly than mechanical methods when applied over large areas. The technology of using plants as described in this paper is offered as an economical and more environmentally sound alternative to other methods. This approach to bioremediation would result in radionuclides concentrated in ash, leaving smaller volumes for efficient disposal. Since environmental conditions vary from site to site, one of the many strengths of this method is its applicability to a wide range of terrestrial environments. Plants could be selected and used that are adapted to growing on contaminated sites in any region of the world. Managers could mini- mize transport of radionuclides from the site through plant and soil management, selection of species less palatable to grazing animals and fencing. The proposed use of plants is attractive because it will not contaminate soil with other forms of hazardous waste, nor destroy the soil's integrity, but it is expected to leave the site amenable to further restoration.

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phytoremediation of soil contaminated with low concentrations of radionuclides

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