Assessing
Phytoremediation’s Progress DANIËL VAN DER LELIE ,
J E A N - PAU L S C H W I T Z G U É B E L ,
D AV I D J . G L A S S ,
JACO VANGRONSVELD,
AND ALAN BAKER
United States Europe
in the and
Although commercial success stories abound, an urgent need still exists for more research and demonstration projects.
hytoremediation—using plants and trees to remove or neutralize contaminants—holds great promise for unobtrusively and costeffectively treating soils, groundwater, and wastewaters contaminated with heavy metals, organic xenobiotics, and radionuclides. Although still an emerging technology, the phytoremediation market is fast-growing, especially in the United States and Europe (1). Like any other new approach, phytoremediation will only be accepted if its success is demonstrated. The key factors are low cost (compared to classical remediation techniques) and aesthetic aspects, making it suitable for remediating large contaminated sites in populated areas. U.S. researchers pioneered phytoremediation demonstration projects and can be largely credited for the positive image that phytoremediation has today. As a result of its more conservative attitude toward demonstration projects, only a few successful, welldocumented demonstration projects have been performed in Europe (Table 1). Comparison of recent developments in Europe and the United States shows that efforts to market the technology are somewhat different on the two sides of the Atlantic. Despite differences and a grow-
LOEL BARR
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© 2001 American Chemical Society
ing track record of commercial success, more demonstration projects will be needed to prove that this new green technology works, quantify its underlying economics, and expand applications.
Scope of applications Potential obstacles to large-scale application of phytoremediation technologies include the time required for remediation, the pollutant levels tolerated by the plants used, and the fact that only the bioavailable fraction of the contaminants will be treated. From ecological, toxicological, and health points of view, the bioavailable fraction should be the most important consideration, but present environmental regulations are mainly based on total pollutant concentrations. An example application of a current risk-based phytoremediation concept involves using metal-inactivating soil additives such as coal fly ash or zeolites combined with revegetation. Using these soil amendments strongly reduces the availability of metals to plant uptake and limits eventual toxicity to plants, allowing revegetation of contaminated sites. Establishment of the vegetative cover markedly decreases metal leaching to groundwater and prevents the dispersal of polluted dusts through wind and rain erosion from formerly bare sites (2, 3). NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 447 A
TA B L E 1
European phytoremediation field projects These projects, successfully carried out in Europe, indicate the range of applications possible for cleanup of sites contaminated with heavy metals and organic compounds. Site name, location
Institution
Plant species
Contaminants
Czechowice oil refinery, Katowice, Poland
Phytotech, Florida State University, Institute for Ecology of Industrial Areas
Brassica juncea
Pb, Cd
Former landfill, Switzerland
Swiss Federal Institute of Technology
Salix viminalis (willow)
Zn, Cd
Sewage disposal site, United Kingdom
University of Glasgow
Salix species (willow)
Ni, Cu, Zn, Cd
Zinc waste landfill, Hlemyzdi, Czech Republic
International Graduate School Zittau
H. annuus, C. sativa, Z. mays, C. halleri
Zn
Zinc/copper-contaminated site, Dornach, Switzerland
Several
Improved tobacco plants
Cu, Cd, Zn
Zinc/cadmium-contaminated playing ground, Overpelt, and zinc smelter site, Lommel, Belgium
Limburgs University
Grasses for phytostabilization
Zn, Cd, Pb, Cu
Zinc/cadmium-contaminated soil, Balen, Belgium
Limburgs University
Brassica napus for phytoextraction
Zn, Cd, Pb
Oil well blowout, Trecate, Italy
Battelle Europe
Alfalfa, clover, corn, rye, sorghum, and soy
Petroleum hydrocarbons
BTEX-contaminated groundwater, Ghent, Belgium
Limburgs University
Populus x canadensis (poplar)
BTEX (benzene, toluene, ethylbenzene, xylene)
In contrast, phytoextraction requires the availability of metals to plants. In fact, amending the soil with chemical chelators that increase metal bioavailability, uptake, and translocation in plants has been proposed as a way to overcome bioavailability limitations, but this necessitates careful mass balances to confirm that metals mobilized by chelators are not leached to groundwater. Using synthetic chelator chemicals is a questionable practice from an environmental standpoint. Natural chelators of plant or microbial origin seem more promising. Microbial protection of plants against phytotoxic concentrations, however, is often based on exclusion of heavy metals, and therefore, it is uncertain whether an approach based on chemical chelators is practical for improving phytoremediation. Broadening the technology’s applicability will require using plants that perform better. This is particularly true for phytoremediating metals, which requires plants with high biomass production and heavy metal uptake and translocation capacities. Plants phytoremediating organic xenobiotics would also need increased degradation potential. Use of genetically modified plants and organisms is conceivable, but this approach must consider the safety of 448 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001
modified plants, potential risks of transferring contaminants to the food chain, and environmental impacts. An alternative phytoremediation enhancement strategy might rely on improved interactions between plants, rhizospheric bacteria, and mycorrhizal fungi, an approach that often assists plants in overcoming toxicity problems. The economics of phytoremediation is generally favorable but can be improved. One option is using plants that provide added value by producing biomass. For example, oil- or fragrance-producing plants such as vetiver, lavender, or coriander could be used and their valuable oil and fragrance products recovered. Alternatively, combustion can reduce the volume of contaminated biomass, followed by selective recovery of heavy metals from residual ash. Depending on the type and concentration of the metal, this could provide an economically valuable recycled product. In developing phytoremediation strategies, preharvest parameters (type and degree of pollution, plant selection, treatability, agronomic techniques, groundwater capture zone, uptake rate, transpiration rate, and required cleanup time) and postharvest evaluation parameters (collection, residues, waste dis-
posal, and contaminated plant material treatment) must be considered. The success of phytoremediation thus depends on many biological, physical, and chemical parameters with help from plant physiologists, agronomists, soil scientists, and engineers. Creating multidisciplinary project teams to accomplish these tasks depends on funding opportunities, and it is in this arena that differences between United States and European phytoremediation approaches become evident.
Funding Substantial funding has been allocated to phytoremediation research in the United States and Europe, although the driving forces behind the type of research performed in each of these markets differ. In Europe, phytoremediation research has been more basic research-driven, with applications determined by research outcomes. In the United States, phytoremediation research has always been more application- and experience-driven. This may reflect a U.S. culture supportive of entrepreneurship and risk taking in business ventures, thereby accounting for a larger, more mature phytoremediation industry and a greater emphasis on applied research, even within academia. Another explanation could be differences in the types of funding support. In Europe, the major opportunities involve basic and exploratory research, although the increasing tendency is for more applications-driven research, as demonstrated by several phytoremediation projects presently supported by the European Commission (EC) 5th Framework Program (1999–2002): • The Phytodec project is a decision support system for quantifying the costs and benefits of using vegetation for managing metal-polluted soils and dredged sediments. • Another project, Phytoc, evaluates willow plantations for phytorehabilitation of contaminated arable land and floodplain areas. • Myrrh considers mycorrhizal fungi for phytostabilizing radionuclide-contaminated environments. • Mycorem explores whether mycorrhizal fungi occurring at naturally contaminated sites confer tolerances to crop plants in soils polluted by heavy metals, salts, and polycyclic aromatic hydrocarbons. • Endegrade examines the use of endophytic bacteria to improve plant degradation of organic xenobiotics. • Last, Piramid combines artificial wetlands and subsurface reactive barriers for passive in situ remediation of acidic mine and industrial drainage. Phytoremediation also received some support during the previous 4th Framework Program (1995–1998). These projects, which were more driven by basic research than the projects presently funded by the EC, included the following undertakings. • Phytorehab compared strategies for rehabilitating metal-polluted soils, including in situ phytoremediation, immobilization, and revegetation. • Biorenew studies biomass fuel crops for bioremediating economic renewing degraded industrial lands. • Phytorem addressed phytoremediation of metalcontaminated soil in a controlled land treatment unit
and was aimed at designing a suitable containment system for safe application of metal chelators. • Rhizodegradation investigated an integrated concept for in situ remediation of hydrocarbons in soil through enhanced degradation by rhizospheric microorganisms. Over the past few years, however, European research also has stronger involvement of small- and medium-sized business enterprises. This might reflect a general tendency to support more applicationsoriented research. EC-funded phytoremediation research is mostly aimed at heavy metals contamination, despite the fact that soil and groundwater pollution by organic xenobiotics is a much more serious problem. Industrial funding for phytoremediation research has been very limited in Europe, and in general, much of the long-term, ongoing research started in Europe has been very broad-based research, supported by
(a)
(b)
Thissite atM aatheide,Belgium ,heavilycontam inated w ith Zn,Cd,and Pb,isshow n here (a)before and (b)after phytostabilization using a 5% beringite soiladditive. NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 449 A
national funding. Research has only recently been directed to phytoremediation applicability, due to new funding opportunities. In Europe, some coordination of phytoremediation efforts at the level of national research projects and a successful network have been established under the framework of COST Action 837 (http://lbewww. epfl.ch/COST837), a unique European initiative established at the end of 1998. Several American programs foster cooperation of various kinds, but they often lack the interdisciplinary approach that COST has assembled. In fact, a common complaint in the United States among remediation professionals and researchers alike is that engineers with remediation expertise and experience do not always communicate with scientists who understand the underlying basis of the remediation approach. The ability of COST Action 837 to bring together researchers with different backgrounds is unique in this respect. Early research on phytoremediating organic contaminants in the United States started in entrepreneurial companies like Ecolotree, Phytokinetics, and Applied Natural Sciences. Some early applicationsoriented research was conducted and funded by the U.S. EPA. In spite of long years of pioneering basic research on hyperaccumulation, metals phytoremediation did not reach its current established level in the United States until the mid-1990s, with the founding of Phytotech. Most U.S. phytoremediation research is government funded—traditional federal support of academic research, small business grants to companies for applied research, and funding of remediation projects. Basic phytoremediation research is most commonly funded by individual competitive grants awarded by government agencies, including EPA, the U.S. Department of Agriculture (USDA), and the U.S. Department of Energy (DOE). Individual research projects more specific to a given remediation problem are funded by these agencies, as well as by various services within the U.S. Department of Defense (DOD). Several programs within or among agencies, such as the DOD/DOE/EPA Strategic Environmental Research and Development Program (SERDP) and DOD’s Environmental Security Technology Certification Program have actively funded phytoremediation laboratory and field projects. Because the funding comes from divisions of these agencies devoted to solving real-world environmental problems, the projects by their very nature are more applications-focused. A limited number of larger-scale funding programs in the United States focuses on phytoremediation. EPA has funded phytoremediation research at the Great Plains/Rocky Mountain Hazardous Substance Research Center (HSRC) for about 10 years. Although this program is based at Kansas State University, funds have been distributed to 14 U.S. universities. In September 2000, a competitive phytoremediation grant program was announced as a joint effort of EPA, the National Science Foundation, the Office of Naval Research, and SERDP. Applications were solicited for field research projects addressing the fundamental interaction mechanisms among microorganisms, 450 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001
Phytostabilization of heavy metal-polluted soils, with or without addition of soil additives, is a proven technology. plants, and contaminants in soils and sediments that result in the degradation, extraction, volatilization, or stabilization of waste chemicals. The program encourages collaborations of life scientists with engineers, and it is hoped that projects will take place on existing field sites controlled by the funding agencies. At this writing, no grants have been awarded. Industrial and private phytoremediation work in the United States is also supported. Although it is a larger effort than in Europe, we are not aware of published figures quantifying relative amounts of spending on phytoremediation research in the American public and private sectors. Information on amounts of industrial funding is often confidential and hard to obtain. Many field phytoremediation projects undertaken in the United States have been conducted at sites owned by private companies, either as pilot research projects or as part of actual remediation efforts. Various chemical and petroleum companies have led these efforts (4, 5), as well as industrial consortia, such as the Petroleum Environmental Research Forum and the International Lead and Zinc Research Organization.
Applications and needs Phytostabilization of heavy metal-polluted soils, with or without addition of soil additives, is a proven technology, as indicated by the many successful studies in both Europe and the United States. In Europe, one of the most successful examples was the use of beringite for treating a site heavily contaminated with Zn and Cd at Maatheide, Belgium (see photos on previous page). Beringite is a modified aluminosilicate that originates from the fluidized bed burning of coal refuse from the former coal mine of Beringen (Belgium). The high metal immobilizing capacity of beringite is based on chemical precipitation, ion exchange, and crystal growth. Unfortunately, this additive is no longer available. Several studies are seeking alternatives. Although these initiatives are strongly supported by regional and national governments, indicating their willingness to accept in situ immobilization as a remediation strategy, most recognize a need for cost-effective systems to monitor the sustainability of phytostabilization (3). Because physical, chemical, and ecological parameters were all evaluated at the Maatheide site during the past decade, it provides an excellent example of the sustainability of heavy metal immobilization combined with revegetation (2). Similar experiments have been performed near a copper rod plant in Prescot, United Kingdom (6).
Phytoextraction of heavy metals has been successfully applied, mostly in the United States. The most publicized example was Phytotech’s (now part of Edenspace Corp.) phytoextraction of lead at a Superfund site in New Jersey—a facility formerly operated by a battery manufacturer (7 ). Phytotech has also phytoremediated a lead-contaminated site in Bayonne, NJ, and at a residential site in Dorchester, MA. Phytomining of nickel is newer. Its primary aim is cost-efficient nickel mining instead of decontamination. Nickel has a high value on the world market, compared with other heavy metal contaminants, such as cadmium, zinc, and lead. Moreover, several high biomass-producing natural nickel-hyperaccumulator plants such as the South African Berckheya roddii are available. Recently, a hyperaccumulator fern (Pteris vittata) was discovered for arsenic, which could also lead to interesting applications (8). An ideal plant for metal phytoextraction is tolerant to accumulated metal concentrations and accumulates metal(s) in aboveground leaves and stems. It should also have fast-growing biomass that is highly metal-accumulating and easily harvested (9). In addition, genetic engineering of plants opens up new possibilities for phytoremediating metal-polluted soils. Several metal transporter genes from small hyperaccumulator plants have been characterized, and these may be a potential source of genes for high biomass-producing hyperaccumulators. Another strategy for remediating metals involves introducing gene-encoding enzymes (often bacterial) that detoxify metals by changing their redox state or by chemically converting them into less hazardous compounds. Phytoremediating organic xenobiotics is becoming increasingly popular as an unobtrusive, costeffective remediation strategy and is enjoying considerable commercial use and success in the United States. Several European and U.S. academic research teams are working to unravel the mechanisms underlying uptake, transformation, and accumulation of organic pollutants, such as pesticides, chlorinated solvents, and sulfonated aromatic compounds released by dye and textile industries. It is becoming increasingly clear that plants contain a complex array of enzymes that can detoxify herbicides and other xenobiotics (10–12). Plants readily take up moderately hydrophobic soil contaminants having log Kow values between 0.5 and 3.5, and rhizospheric microorganisms can degrade more hydrophobic pollutants. More research is required to better understand and exploit the interactions between plants, microorganisms, and organic xenobi-
Phytoremediating organic xenobiotics is becoming increasingly popular as an unobtrusive, cost-effective remediation strategy.
otics and to use this information to improve phytoremediation efficiency in the field. Although many organic pollutants are metabolized in plants, some xenobiotics can be toxic, limiting the applicability of phytoremediation. Moreover, in phytoremediating volatile organic chlorinated compounds, BTEX (benzene, toluene, ethylbenzene, xylene), and MTBE (methyl tert-butyl ether) plants can release the compounds and their metabolites to the atmosphere, which udermines the merits of phytoremediation for these applications. This problem has prompted several researchers to examine alternative strategies, including the use of improved rhizodegradation. However, although rhizospheric microorganisms can improve phytoremediation of hydrophobic compounds, such as hydrocarbons, recent results suggest that numerous compounds enter the plant faster than soil microflora can degrade them (13). A study of phytoremediation of hydrocarbon-polluted agricultural soils that was successfully conducted in Trecate, Italy, is instructive (14). Soil contaminated following a blowout of a land-based oil well underwent treatment in a biopile before being replaced in its original location. During three growing seasons, the ability of 11 agricultural plants to stimulate hydrocarbon removal via microbial degradation and plant uptake was compared with land farming and natural attenuation. Total petroleum hydrocarbon reduction during the third season ranged from 0.21 to 0.57 kg/m2 in planted parcels, whereas the average reduction in land-farmed parcels was only 0.01 kg/m2. Maize and sorghum were very efficient for such applications. Other hydrocarbon phytoremediation projects are under way in Europe (13). A special phytoremediation application is constructed wetlands for cleanup of effluents and drainage waters. For example, a constructed wetland near Aveiro in Portugal has successfully treated industrial effluents containing nitrogenous aromatic compounds from an aniline and nitrobenzene production plant for several years (project Reciclam). Up to 100% reductions in aromatic compounds are obtained using reed beds on a total planted area of 10,000 m2. The reduction efficiency depends on the acclimatization period for inlet effluent compositions of 10–300 mg/L aniline, 10–100 mg/L nitrobenzene, and 10–30 mg/L nitrophenols. The U.S. Army Corps of Engineers, Waterways Experiment Station in Vicksburg, MS, is developing a wetlands system to treat groundwater contaminated with 1 mg/L TNT (2,4,6-trinitrotoluene) and up to 13 mg/L RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine). Laboratory studies led to the selection of three aquatic species: coon-tail (Ceratophyllum demersum), pondweed (Potamogeton nodosus), and emergent arrowhead (Sagittaria latifolia), which all reduced TNT levels by 95%, and RDX by 80%. It is believed that remediation using these species involves endogenous enzyme systems (nitroreductase, dioxygenases, and laccase). A full-scale trial has been initiated (15, 16). Radionuclide phytoremediation is less well documented, but some trials have been performed. Laboratory and greenhouse studies have determined NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 451 A
Radionuclide phytoremediation is less well documented, but some trials have been performed. the phytoremediation potential for removing low levels of Cs-137 at a former waste disposal site at Argonne National Laboratory’s facility in Idaho. Willow, Kochia scoparia (a weedy plant) and Brassica napus (colza) were tested on spiked soil and found capable of 40–60% removal of Cs-137 under greenhouse conditions. The results suggest that four to seven years would be needed for field remediation at this particular site. MSE, Phytotech, and the Cornell– USDA group have also conducted laboratory and initial field studies on removal of Cs-137 from contaminated soils. Studies in pots identified species from the mustard (Brassicaceae) and amaranth (Amaranthaceae) families that could accumulate threefold more Cs-137 in leaf and stem biomass than concentrations present in test soils. In field trials, redroot pigweed (A. retroflexus L.) showed the best performance, accumulating ⬎900 pCi/g, well over the goal of 300 pCi/g. Phytotech also conducted a field trial of rhizofiltration, using sunflowers in a greenhouse-based hydroponic reactor, and found that uraniumcontaminated water at concentrations ≤350 µg/L could be reduced 95% within 24 hours. Concentrations of uranium in roots were 5000–10,000 times greater than water. Using sunflowers grown on rafts in a contaminated pond, Phytotech conducted a field trial on surface water contaminated with Cs-137 and Sr-90 from the Chernobyl, Ukraine, nuclear accident and showed a dramatic reduction in radionuclide levels in the water in a four- to eightweek period. In 12 days, plant roots had Cs and Sr concentrations 8000- and 2000-fold higher than groundwater, respectively.
Outreach Initiatives have been undertaken to improve the dissemination of results to the general public and the science community. The most significant are the Phytonet discussion group (www.dsa.unipr.it/ phytonet), the EPA’s Citizen’s Guide to Phytoremediation (http://cluin.org/products/citguide/phyto2. htm), and a forthcoming publication by the Interstate Technology and Regulatory Cooperation Working Group, which explains phytoremediation and its applications primarily for state and local regulators. In addition, the Kansas State University HSRC program sponsors the Phytoremediation Discussion Group (www.engg.ksu.edu/HSRC/phytorem). These undertakings primarily target the scientific community rather than the general public and are aimed at creating discussions among scientists from different disciplines. Overall, the message is that there 452 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001
is an urgent need for research aimed at fundamental understanding of mechanisms involved in soil and plant compartments and demonstration projects to optimize the phytoremediation process and convince regulators and the general public of the technique’s applicability.
Acknowledgment D.v.d.L. is supported by Laboratory Directed Research and Development funds at the Brookhaven National Laboratory under contract with the U.S. Department of Energy.
References (1) Glass, D. J. U.S. and International Markets for Phytoremediation, 1999–2000; D. Glass Associates, Inc.: Needham, MA, 1999. (2) Vangronsveld, J.; Colpaert, J.; van Tichelen, K. Environ. Pollut. 1996, 94, 131–140. (3) Tibazarwa, C.; Corbisier, P.; Mench, M.; Bossus, A.; Solda, P.; Mergeay, M.; Wyns, L.; van der Lelie, D. Environ. Pollut. 2001, 113, 19–26. (4) Huang, J. W.; Chen, J.; Cunningham, S. D. Phytoextraction of lead from contaminated soils. In Phytoremediation of Soil and Water Contaminants; Kruger, E. L., Anderson, T. A., Coats, J. R., Eds.; ACS Symposium Series No. 664.; American Chemical Society: Washington, DC, 1997; pp. 283–298. (5) Tsao, D. The industrialist’s perspective—Can phytoremediation really deliver what industry needs? In IBC’s 4th Annual International Conference on Phytoremediation, Toronto, Ontario, Canada; June 23–25, 1999; International Business Communications: Southborough, MA, 1999. (6) Rebedea, I. Ph.D. Thesis, John Moores University, Liverpool, United Kingdom, 1997. (7) Blaylock, M. J. Phytoremediation of lead-contaminated soil at a brownfield site in New Jersey—A cost-effective alternative. In IBC’s 2nd Annual International Conference on Phytoremediation, Seattle, WA, June 18–19, 1997; International Business Communications: Southborough, MA, 1997. (8) Ma, L. Q.; Komar, K. M.; Tu, C.; Zhang, W.; Cai, Y.; Kennelley, E. D. Nature 2001, 409, 579. (9) Reeves, R. D.; Baker, A. J. M. Metal-accumulating plants. In Phytoremediation of toxic metals—Using plants to clean up the environment; Raskin, I., Ensley, B. D., Eds.; Wiley and Sons: New York, 2000; pp. 193–229. (10) Coleman, J. O. D.; Blake-Kalff, M. M. A.; Davies, T. G. E. Trends Plant Sci. 1997, 2, 144–151. (11) Edwards, R.; Dixon, D. P.; Walbot, V. Trends Plant Sci. 2000, 5, 193–198. (12) Werck-Reichhart, D.; Hehn, A.; Didierjean, L. Trends Plant Sci. 2000, 5, 116–123. (13) Trapp, S.; Karlson, U. J. Soils Sed. 2001, 1, 1–7. (14) Plata, N. Ph.D. Thesis Nr 2306, EPFL, Lausanne, Switzerland, 2000. (15) Hughes, J. B.; Shanks, J.; Vanderford, M.; Lauritzen, J.; Bhadra, R. Environ. Sci. Technol. 1997, 31, 266–271. (16) Thompson, P. L.; Ramer, L. A.; Schnoor, J. L. Environ. Sci. Technol. 1998, 32, 975–980.
Daniël van der Lelie is a senior scientist at Brookhaven National Laboratory, Upton, NY. Jean-Paul Schwitzguébel is senior scientist at the Swiss Federal Institute of Technology Lausanne, Laboratory for Environmental Biotechnology, Lausanne, Switzerland and the chair of COST Action 837. David J. Glass is the chief executive officer at Applied PhytoGenetics, Inc., Athens, GA, and head of D. Glass Associates, Inc., Needham, MA. Jaco Vangronsveld is a professor at Limburgs Universitair Centrum, Centre for Environmental Sciences, Diepenbeek, Belgium. Alan Baker is professor at the University of Melbourne, Parkville, Victoria, Australia.
