Phytoremediation and Reclamation of Soils ... - ACS Publications

Chapter 22

Phytoremediation and Reclamation of Soils Contaminated with Radionuclides 1

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Downloaded by UNIV MASSACHUSETTS AMHERST on October 6, 2012 | http://pubs.acs.org Publication Date: April 8, 1997 | doi: 10.1021/bk-1997-0664.ch022

James A. Entry , Lidia S. Watrud , Robin S. Manasse , and Nan C. Vance

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Department of Agronomy and Soils, College of Agriculture, 202 Funchess Hall, Auburn University, Auburn, A L 36849-5412 Terrestrial Plant Ecology Branch and National Research Council, National Health and Environmental Effects Laboratory, U.S. Environmental Protection Agency, 200 Southwest 35th Street, Corvallis, OR 97333 Pacific Northwest Research Laboratory, Forest Service, U.S. Department of Agriculture, 3200 Jefferson Way, Corvallis, OR 97331 2

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As a result of nuclear testing and nuclear reactor accidents, large areas of land have become contaminated with low concentrations of radionuclides. Removal, transport and treatment of large volumes of soil may be logistically difficult and prohibitively costly. Using plants to remove low concentrations of radionuclides from soil in situ is expected to be less expensive than mechanical, physical or chemical methods, particularly for treatment of large areas. Phytoremediation is applicable to a wide range of terrestrial environments and plants can be selected for given soil and climatic conditions. Phytoremediation of contaminated sites should also leave treated sites amenable to subsequent reclamation efforts. The points to consider for initial phytoremediation and subsequent reclamation of contaminated soils include:enhancement of plant accumulation of radionuclides by addition of mycorrhizal or bacterial inocula, chelating agents or organic amendments, periodic harvests to recover or dispose of radionuclides in the ashed plant materials minimization of potential environmental effects on non-target organisms and replacement or augmentation of the initial remediating species with a complex plant community. Large areas of land have been contaminated by fission by-products resulting from nuclear bombs, (1) above ground nuclear testing (2-4), nuclear reactor operations (5, 6) and nuclear accidents (7). Unlike organic pollutants, radionuclides typically are elements which cannot be degraded. Radionuclides can be distributed to soil and plants in the contaminated area by physically and biologically mediated nutrient cycling processes (8 -11). Radionuclides, especially Cs and ^Sr, can accumulate as they move up the food chain (12). Significant concentrations of radionuclides have been found in crops (4,13,14), livestock (14), fish (5, 15) and wildlife (16, 17). Human exposure to harmful 137

© 1997 American Chemical Society

In Phytoremediation of Soil and Water Contaminants; Kruger, E., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1997.

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PHYTOREMEDIATION OF SOIL AND WATER CONTAMINANTS

radionuclides can occurfrominhalation following atmospheric releases, or by ingestion of food contaminated by atmospheric fallout or by accumulation through the food chain (18). Exposure may result in detrimental health effects, such as cancers and genetic mutations (9, 19, 20). This chapter provides an overview of the current progress in phytoremediation of radionuclides from soils and will propose a strategy for initial remediation, (ie. reduction of contaminant levels and subsequent reclamation or revegetation of impacted areas).


Benefits of Phytoremediation Remediation of soil contaminated with low concentrations of radionuclides using present technology requires that soil be removedfromthe contaminated site and treated with various dispersing and chelating chemicals. Transport of soil requires heavy equipment, is time consuming and expensive; it may also result in additional dispersal of pollutants through possible spill and/or leaks. Therefore, few attempts have been made to remediate large areas of land contaminated with low concentrations of radionuclides. Furthermore, the cost to dispose of large liquid volumes of chemicals used to decontaminate soils polluted with radionuclides may be prohibitive; estimates of $200 to $300 billion for radionuclide cleanup in the U. S. alone, are considered conservative (21). In addition to the logistical and cost limitations for treating soils with present technology, physical and chemical alteration of soils may inhibit reclamation ofthe site. The heavy equipment needed to remove or transport soil compacts the remaining soil, adversely affecting the porosity, bulk density and water holding capacity of soil. Changes in aeration and water availability can in turn negatively impact plant growth and nutrition. If the soil is returned to the site, use of dispersing compounds such as detergents and surfactants and chelating agents during soil washing procedures to extract pollutantsfromsoil can promote the loss of soil nutrients and cofactors needed by plants, microbes and other soil biota. In large quantities, chelating compounds may also adversely affect soil physical characteristics such as cation exchange capacity. Surfactants and detergents may adversely affect the viability of prokaryotic and eukaryotic soil biota by causing membrane damage. The establishment of plants on physically, chemically and microbiologically compromised soils can therefore become problematic. In contrast, phytoremediation-based approaches, particularly those designed with planned, successive in situ harvests and simultaneous or sequential perimeter plantings of other species, may not only remediate a site, but may eventually reclaim it, by fostering the establishment of a plant community. The ensuing sections will (a) review plant species that have been evaluated for in situ phytoremediation of radionuclides in contaminated soils, (b) propose criteria for selecting and developing plant species to be used for phytoremediation, (c) suggest points to consider for minimizing non-target effects of plants and (d) highlight basic and applied research needed to help ensure environmental and human safety, as well as efficacy of phytoremediation.


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Reclamation of Soils Contaminated with Radionuclides 301 137

Survey of Plants that Accumulate Cs and '"Sr Although the ability to accumulate radionuclides varies among a wide array of plant species occupying different habitats, many plants growing on contaminated soils have been shown to accumulate large amounts of radionuclides. Numerous reports have described plant accumulation of radionuclides, especially Cs and Sr (14, 22-25). Laboratory experiments indicate that certain plants may be able to remove radionuclides, especially Cs and ^Srfromsoil over a time period of 5 to 20 years. Nifontova et al. (6) found that plants accumulated between 530 and 1500 Bq of Cs and between 300 and 1100 Bq of Sr over a 10 year period 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 (22) found that a large number of plant species in the desert area near the Nevada Test Site, USA, accumulated substantial quantities of radionuclides from soils contaminated by above-ground nuclear testing. Trees can also accumulate substantial quantities of radionuclides. Pinder et al. (23) reported that Acer rubrum, Liquidambar stryaciflua and Liriodendron tulipifera accumulated significant quantities of Cm, Cs, Pu, Ra and Sr. Robison and Stone (4) found that Cocos nucifera accumulated substantial amounts of Csfromsoils contaminated by nuclear weapons testing on Bikini Atoll. They also reported that additions of Κ and Ρ to the soil decreased the amount of Cs taken up by the trees. Entry et al (26) found that Pinus radiata and Pinus ponderosa seedlings accumulated substantial quantities of Cs and Sr. Entry and Emmingham (27) found that potted Eucalyptus tereticornis seedlings removed 31.0 % of the Cs and 11.3 % of the Sr in sphagnum peat soil after one month of exposure. Accumulation of Cs and ^Sr in grasses and other herbaceous plants has also been widely documented. Dahlman et al. (28) reported that Festuca arundinacea accumulated 42,143 kBq of Cs m" in 8 months, in an area where the total amount of Cs above-ground runoff and sediment was less than 444 kBq of Cs. Salt et al. (14) reported that Lolium perenne, Festuca rubra, Trifolium repens and Cerastium fontanum accumulated from 28 to 1040 Bq Cs g of plant tissue in a re-seeded pasture in Scotland. Coughtery et al. (24) found that a Festuca / Agrostis plant community in the United Kingdom accumulated 4-19% of the Cs deposited by Chernobyl fallout. Accumulation of Cs was higher in Carex spp than in 9 species of grasses in an upland area in Great Britain (24). Radionuclides such as Sr and Cs often accumulate as they move up the food chain. Radionuclides are accumulated by zooplankton, aquatic plants, fungi and invertebrates such as earthworms. Penntilla et al (15) reported that Cs and Sr bioaccumulation in aquatic and terrestrial animals that consume plants eventually leads to incorporation into many foods consumed by humans. Haselwandter and Berreck (29) have recently reviewed accumulation of radionuclides by arbuscular mycorrhizal and ectomycorrhizal fungi and their bioaccumulation in the food chain. 137

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Criteria and Approach for Selecting Candidate Phytoremediation Species Candidate plant species to remove radionuclidesfromcontaminated soils can be selected and evaluated for efficacy and for environmental safety by using a multi-staged screening approach (30). The first step is to identify plant species or cultivarsfromthe literature or from contaminated sites for their potential abilities to take up given radionuclides. Subsequent points to consider for revegetation of damaged terrestrial ecosystems include assessment of potential ecological effects, agronomic requirements and reproductive characteristics (31, 32). Specific examples of points to consider in selecting or developing plant species for remediation, reclamation or restoration purposes are summarized in Table I. For example, major ecological considerations should address (a) therisksand benefits of using native or exotic species (b) ability of the introduced plants to hybridize with other species, especially weeds, (c) whether the plants are insect or wind pollinated and (d) whether the species are annuals or perennials and (e) effects of concentrated radaionuclides on potential herbivores and pollinators. Agronomic considerations should take into account biomass production, water, nutrients and cultural requirements; ability to form beneficial associations with mycorrhizal fungi, nitrogen fixing or other plant growth promoting soil or rhizobacteria; tolerance to disease, insects and temperature; and to salt or pH extremes. Reproductive considerations should include seed and pollen production. Morphology of the root system and its ability to penetrate and spread in different soil types could be important both in maximizing uptake of radionuclides or other pollutants, and in stabilizing the soil to minimize aerial dissemination of contaminated soils. Some of these properties can be tested in the greenhouse using soils representative of contaminated sites. The effects of organic amendments and mycorrhizal or other microbial inoculants on efficacy can be evaluated initially in greenhouse tests and later in field tests. Similarly, effects on non-target organisms can be tested initially in greenhouse systems and later under field conditions. Minimizing Non-Target Ecological Effects of Phytoremediation Practices Ecologicalriskfromweedy or invasive species can be minimized with precautions. For example, the potential for hybridization with weeds and for pollen and seed dissemination can be reduced by harvesting before flowering or seed set. In the future, using infertile hybrids or sterile males of selected species may be a viable option. Avoidance of insect pollinated plants can reduce exposure of accumulated toxics to insect pollinators such as bees, butterflies or other insects. Selecting plants that are less palatable to grazing by vertebrate or invertebrate herbivores, and wind-pollinated rather than insect-pollinated plants, reduces the potential for food-chain accumulation. Periodic harvests of the above-ground portion of plants may maximize continued uptake, reduce potential phytotoxicity associated with bioaccumulation and reduce exposure to potential pollinators, and to vertebrate and invertebrate herbivores. By reducing the potential for phytotoxicity to the accumulating species, the useful life of a given planting may be increased, thereby reducing the need for re-seeding or replanting.


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Strategy for In Situ Phytoremediation of Radionuclide Contaminated Soils


Soil Amendments The most desirable soil conditions are those that enhance plant uptake of radionuclides without increasing radionuclide mobility in the soil. Achieving this condition in soils in situ may be approached in two ways: 1) by improving the ability of the plant to take up radionuclides, (eg., via mycorrhizal associations) (29, 33) or by inoculation with plant-growth promoting rhizobacteria (34, 35), and /or 2) by altering the chemical form of the radionuclide in the soil to increase its availability to plants. Table I. Points to Consider in Selecting Plants for Phytoremediation Purposes A. Ecological Aspects

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Native or exotic species Invasiveness Ability to hybridize with weed species Wind or insect dissemination of pollen Potential impacts on herbivores Longevity

B. Agronomic Considerations

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Availability of seeds or transplants Biomass production Fertilizer requirements Water requirements Availability of harvesting methods Suitability for multiple harvests Disease and insect tolerance Potential for symbiotic associations Types of suitable soils and climates Tolerance to environmental stresses

C. Reproductive Characteristics

• Seed production and viability • Pollen production

D. Efficacy and Economics

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Effective limits of remediation Time required for adequate remediation Harvest, recovery and disposal costs Potential for recovery of pollutants Costs for re-seeding or re-planting

Inoculation of plants or soil with specific mycorrhizal fungi or other root associated microflora may additionally maximize plant uptake and accumulation of radionuclides (30). The availability of radionuclides to plants can be enhanced, while decreasing the mobility of these radionuclides in soil, by in situ addition of organic


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amendments, and carefully managed concentrations of chelating agents and fertilizer (30). Chelators, such as diethylenetriamine-pentaacetic acid (DTPA), alter the radionuclide form so it is more biologically available to the plant but not increasing its mobility to the point where it is easily leachfromthe soil. Organic matter will complex with Cs and *°Sr to remove themfromabsorption sites on mineral solids and reduce soil pH and base saturation, thereby increasing 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. Mechanisms proposed for the binding include oxygen bonds, cation bridges and chelated metal bridges (36). If oxygen bonds or other cations are providing bonding to clay sites, then chelated radionuclides should be expected to be accessible for uptake into plants. Harvested plant materials would then be subjected to high temperature combustion or smelting to oxidize and concentrate radionuclides in ash for disposal or recovery.


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Strategy for Reclamation of the Phytoremediated Area In the long term, plants native to an area would be the most desirable from an ecological viewpoint. In nonagricultural lands, if appropriate, the area surrounding the targeted remediation site can be planted with a mixture of seeds from native species. Perimeter plants serve several purposes. They (a) reduce erosion and dissemination of contaminated soil and (b) produce a source of propagules (roots, rhizomes, stolons, seeds, etc.), that can grow in the phytoremediated area and as suggested by Chambers and Mac Mahon (37), facilitate the growth and spread of indigenous or introduced mycorrhizal inocula. With appropriate species selection, one might anticipate that over a period of several years, the species in the phytoremediation area would gradually become replaced by native species. Planting of the perimeter areas could be achieved by mulching with plant canopies from adjacent areas (38). Conventional low cost methods such as tilling and broadcasting or drilling seed, or higher cost transplant methods (of seedlings or of plugs of soil with plantsfromadjacent plant communities) can also be considered, depending on the size of the area to be remediated. Research Needs Numerous research needs exist, ranging from maximization of efficacy in the field to ecological and health effects risk assessment studies. Genetic manipulation of candidate plant species and of associated rhizosphere microflora may be necessary to maximize efficacy while minimizing ecological risks. For example, molecular techniques are available (39), which permit the isolation and introduction of genes to enhance uptake, sequestration, bioaccumulation or biotransformation of given inorganic or organic pollutants (40-43). Plant breeding techniques may be developed that will localize the times or places of radionuclide accumulation in plants to specific plant parts so that environmental exposure to non-target species can be minimized. Cultural and harvest practices aimed at reducing pollen or seed spread, and selection or development of lines with reduced fertility, seed production or seed bank viability may also be useful in minimizing dissemination, persistence and invasion of introduced species. Data are also needed on non-target effects to plant symbionts such as mycorrhizal fungi and nitrogen


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fixing bacteria and on soil foodweb components such as bacteria, fungi, nematodes and protozoans. Research is also needed on toxicity to invertebrate and vertebrate herbivores of above ground and below ground plant parts. Depending on the specific radiological characteristics of given radionuclides, effects on the mutagenicity of the concentrated radionuclides to target and non-target plants, microbes, invertebrates and vertebrates may also need to be addressed. Literature Cited 1. Mahara, Y . J. Environ. Qual. 1993, 22, 722-730. 2. Paasikallo, A . Ann. Agric. Fenn. 1984, 23, 109-120. 3. Eisenbud, M. Experimental Radioactivity. 1987, Academic Press, Orlando, FL, pp 475. 4. Robison, W.L.; Stone, E.L. Health Physics 1992, 62, 496-511. 5. Whicker, F.W.; Pinder, J.E.; Bowling, J.W.; Alberts, J.J.; Brisbin, Jr., L. Ecol. Monogr. 1990, 60, 471- 496. 6. Nifontova, M.G.; Kulikov, G.I.; Tarshis, G.I.; Yachenko, D. Ekologiya 1989, 3, 40-45. 7. Clark, M.J.; Smith, F.B. Nature 1988, 332, 245-249. 8. Abbott, M.L.; Rood, A.S. Health Physics 1994, 66, 17-29. 9. Breshears, D.D.; Kirchner,T.B; Whicker, F.W. Ecol. Appl. 1992, 2, 285-297. 10. Howard, B.J.; Bresford, N.A.; Hove, K. Health Physics 1991, 61, 715-722. 11. Berg, M. T.; Shuman, L. Ecological Modeling 1995, 83, 387-404. 12. Hoffman, F.O.; Bergstrom, U . ; Gyllander, C. Α.; Wilikins, A . B . Nuclear Safety 1984, 25, 533-546. 13. Sanzharova, D.I.; Aleksakhin, R . M . Pochvovedeniye 1982, 9, 59-64. 14. Salt, C.A.; Mayes, D.; Elston, A . J. Appl. Ecol. 1992, 29, 378-387. 15. Pennttila, S.; Kairesalo, T.; Uusi-Rauva, A . Environ. Pollut. 1993, 82, 47-55. 16. Lowe, V.P.W.; Horrill, A.D. Environ. Pollut. 1991, 70, 93-107. 17. Rickard, W.H.; Ebrhard, L.E. Northwest Sci. 1993, 67, 25-31. 18. Church, B.W.; Wheeler, D.L.; Campbell, C.M.; Nutley, R.V.; Ansphaugh, L.R. Health Physics 1990, 59, 503-510. 19. Ansphaugh, L.R.; Catlin, R.J.; Goldman, M. Science 1988, 242, 1513-1519. 20. Lange, R.; Dickerson, M.H.; Gudiksen, P.H. Nuclear Technology 1988, 82, 311223. 21. Watson, R.; Glick, D.; Horsenball, M . ; McCormick, J.; Begley, S.; Miller, S.; Carroll, G.; Keene-Osborn, S. Newsweek, December 27, 1993, pp 14-18. 22. Wallace, Α.; Romney, E . M . Radioecology and Ecophysiology of Desert Plants at the Nevada Test Site. 1972, Environmental Radiation Division, Laboratory of Nuclear Medicine University of California, Riverside, pp 432. 23. Pinder, J.E. III; McLeod, K.W.; Alberts, J.J.; Adriano, D.C.; Corey, J.C. Health Physics 1984, 47, 375-384. 24. Coughtry, P.J.; Kirton, J.A.; Mitchell, R.B. Environ. Pollut. 1989, 62, 281-315. 25. Murphy, C.E.; Johnson, T.L. J. Environ. Qual. 1993, 22, 793-799. 26. Entry, J.A.; Rygiewicz, P.T.; Emmingham, W.H. J. Environ. Qual. 1993, 22, 742-746.



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