Environ. Sci. Techno/, 1995, 29, 1239-1245
Rhirofiltration: The Use of Plants To Remove Heavy Metals from Aqueous Streams VIATCHESLAV D U S H E N K O V , + P. B. A. NANDA KUMAR,+ HARRY M O T T O , # A N D I L Y A R A S K I N * f t AgBiotech Center and Department of Environmental Sciences, Rutgers University, Cook College, P.O. Box 231, New Brunswick, New Jersey 08903-0231
Heavy metal pollution of water is a major environmental problem facing the modern world. Rhizofiltration-the use of plant roots to remove heavy metals from water-is an emerging environmental cleanup technology. Roots of many hydroponically grown terrestrial plants, e.g., Indian mustard (Brassica juncea (L.) Czern.), sunflower (Helianthus annuus L.), and various grasses, effectively removed toxic metals such as Cu2+, Cd2+, C P , Ni2+, Pb2+, and Zn2+ from aqueous solutions. Roots of B,juncea concentrated these metals 131-563-fold (on a D W basis) above initial solution concentrations. Pb removal was based on tissue absorption and on root-mediated Pb precipitation in the form of insoluble inorganic compounds, mainly lead phosphate. At high Pb concentrations, precipitation played a progressively more important role in Pb removal than tissue absorption, which saturated at approximately 100 mg of Pb/g D W root. Dried roots were much less effective than live roots in accumulating Pb and in removing Pb from the solution.
Introduction Heavy metal pollution of aqueous streams is a major environmental problem facing the modern world. Several methods of removing heavy metals from water based on ion exchange or chemical and microbiological precipitation have been developed and used with some success (1, 2). These technologies have different efficiencies for different metals and may be very costly if large volumes, low metal concentrations, and high cleanup standards are involved. Recently, there has been some research into the use of living and nonliving bacteria and algae for the bioremediation and recovery of heavy metals from aqueous streams (3). In addition, live or dead cultured cells of Datura innoxia, a higher plant, can be used to remove Ba2+from solution (4). Commercial applications of this research are still hampered by the high cost of growing pure cultures of cells and microorganisms and by the need for their immobilization or separation from the aqueous stream. Metal-accumulating fungi (5) and Azolla filiculoides, an aquatic fern (6),were also proposed as metal biosorbers capable of remediating industrial effluents. Aquatic higher plants have also been utilized for water purification. Water hyacinth (Eichhornia crassipes) (7,81,pennywort (Hydrocotyle umbellata) (91, duckweed (Lemna minor) (101, and watervelvet (Azollapinnutu) (11)can remove various heavy metals from solution. However, the efficiency of metal removal by these plants is low because of their small size and small, slow-growing roots. The high water content of aquatic plants also complicates their drying, composting, and incineration. In contrast, terrestrial plants develop much longer, fibrous root systems covered with root hairs, which create an extremely high surface area (12). These roots are easily dried in the open air. Here, we demonstrate that hydroponically grown roots of a terrestrial plant Brassica junceu (Indian mustard) effectively remove heavy metals from aqueous solutions. We refer to this process as rhizofiltration, which is defined as the use of plant roots to absorb, concentrate, and precipitate heavy metals from polluted effluents (13).Our estimates indicate that in many cases the efficiency of removal compares favorablywithcurrently employedwater treatment technologies. The commercialization of rhizofltration will be driven by economics as well as by such technical advantages as applicability to many “problem”metals, ability to treat high volumes, lesser need for toxic chemicals, reduced volume of secondary waste, possibility of recycling, and the likelihood of regulatory and public acceptance. B. junceu was chosen as a model plant for rhizofltration because it accumulated high levels of Pb and other heavy metals in a screen that used a number of commercially cultivated plant species (14).In addition, several members of the Brassicaceae family have been shown to accumulate unusually high concentrations of heavy metals in both shoots and roots (15,16). Lead (Pb),cadmium (Cd),copper * To whom correspondenceshouldbe addressed: Telephone: (908) 932-8734;Fax: (908) 932-6535;e-mail address: Raskin@mbcl. rutgers.edu. + AgBiotech Center. Department of Environmental Sciences.
*
0013-936)(/95/0929-1239$09.00/0
0 1995 American Chemical Society
VOL. 29, NO. 5,1995 /ENVIRONMENTAL SCIENCE & TECHNOLOGY rn 1239
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Time (hours) FIGURE 1. Effect of different Pb concentrations on Pb removal from water by the roots of B. juncea. Plants were exposed to 0,35,70,150,
300,and 500 mg of Pb/L (see top of each panel) for 72 h. Controls contained aerated Pb solutions without plant roots. One milliliter aliquots were removedfrom each container and analyzed for metal content using atomic absorption spectrophotometry. Deionized water was added to the metal solution to compensate for the volume removed by sampling. Roots immersed in the solution had an average DW of 0.5 f 0.1 g. Vertical bars denote SE ( n = 4).
(Cu),chromium (Cr),nickel (Ni),and zinc (Zn)were chosen for this study because they are ubiquitous pollutants present in industrial, agricultural, and municipal wastes.
Materials and Methods Plant Material. B. junceu seeds cultivar 173874 were
obtained from the USDAlARS Plant Introduction Station of Iowa State University. The seeds of other plants were purchased from local seed markets or kindly provided by the faculty of the Center for Interdisciplinary Studies in Turfgrass Science at Rutgers University. B. junceu seedlings were cultivated hydroponically with roots growing in aerated nutrient solution [ 1 glL of Hydrosol supplemented with 0.6 g/L Ca(N03)zI. Each hydroponic unit consisted of a PVC plastic cylinder (12 cm tall, 10 cm in diameter), which contained four plants supported by a metallic grid, positioned 7 cm from the bottom and a 1 cm deep layer of 1240 E N V I R O N M E N T A L SCIENCE & TECHNOLOGY/ VOL. 29. NO. 5,1995
vermiculite placed on top of the grid. Eight hydroponic units were placed in a common tray containing 4 L of nutrient solution. After 4-5 weeks, plants were selected for uniformity (average root DW was 0.5 f 0.1 g) except for the experiments shown in Figures 5 and 6. For the experiments with Pb, roots were rinsed for 20 min in deionized water to remove traces of nutrient solution. Thereafter, the cylinder with plants was inserted into a 5 cm deep plastic cup that contained 400 mL of a continuously aerated solution of Pb supplied as Pb(N03)Z. The total volume of the solution was kept constant by adding deionized water to compensate for water lost through plant transpiration, sampling, and evaporation. Experiments were done in an environmentally controlled growth chamber at 25 "C, 75% relative humidity, and 16-h photoperiod (600 pmol m-* s-l) provided by a combination of incandescent and cool-white fluorescent lights. Control treat-
OOQ n v)
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Pb in solution (mg/L) FIGURE 2. Relationship between initial Pb concentration and the time required for B. juncea roots to reduce Pb concentration in the solution by WO.
600
I
-
Concentration in roots Disappearance from solution
I
3
400-
prepared in deionized water. Other broadleaf species, grown similarly to B. junceu, and grasses grown either from seed or from sod were used in the experiments when their dry root weight was between 0.4 and 0.6 g. Dried roots for Pb uptake experiments were prepared by placing excised andwashed roots of B.junceu at 80 “Cfor 2 days. Thereafter, roots were thoroughly rinsed in deionized water and either used in the experiments or redried for later use. Metal Analpis. Heavy metals in root tissue were analyzed using a Fisons direct current plasma spectrometer (DCP) Model SS-7. Roots were dried for 2 days at 80 “C and ashed at 500 “C for 6 h. The ash was dissolved in 2 parts of 1 M HN03 and 1 part of 2 M HC1, and the solution was analyzed by DCP. Lead concentrations in solutions were analyzed directly using a Perkin Elmer 603 atomic absorption spectrophotometer. Other metals in solution were analyzed by DCP. The fact that the amount of metal measured at 0 time was often slightly less than the amount of metal dissolved in solution suggests that some metal was adsorbed to the walls of the experimental container. X-ray absorbance spectroscopy analysis of the oxidation state of Cr in B. junceu roots immersed for 7 days in a solution containing 4 mglL C P was performed at the Stanford Synchrotron Radiation Laboratory (SSRL),Menlo Park, CA. Analysis of root precipitate was performed with a Mattson “Cygnus 100” Fourier-transform infrared spectrometer at 4-cm-’ resolution.
Experimental Results
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To examine the effect of different Pb concentrations on the speed and magnitude of Pb removal, B. junceu plants were grown hydroponically for 4 weeks, selected for uniformity, a 200and exposed to 400 mL of deionized water containing 35500 mglL Pb2+,supplied as Pb(N03)~(Figure 1). The rate of Pb removal depended on the initial Pb concentration in the solution and showed a monotonic decline with time. The loglo of the time required to achieve a 50% reduction in Pb concentration showed a positive linear dependence 0 35 7 0 1 5 0 3 0 0 5 0 0 on the initial Pb concentration in the solution with R2 = Pb in solution (mg/L) 0.99 (Figure 2). It can be estimated from the fitted curve FIGURE 3. Effect of the initial Pb concentration on Pb accumulation that roots immersed in a solution containing 35 mg of Pb/L in B. juncea roots and total Pb removed from solution. Roots were reduced this concentration by 50% in 42 min. A similar exposed to 0,35,70,150,300, and 500 ma of PbL for 72 h. Vertical amount of roots exposed to 500 mg of Pb/L required 43 h bars denote SE (n= 4). to reduce the Pb concentration by 50%. It is important to note that the amount of root tissue used in this experiment ments did not contain roots. A filter paper control (thin was much smaller than could be actually immersed in the strips of filter paper, 0.4 g DW, immersed in the aerated Pb contaminated solution. Since the magnitude of Pb removal solution) was used to demonstrate that Pb uptake is root is proportional to the root weight (see below), much faster specific. Salt solutions of Cd(N03)2*4H20,Pb(NO3I2,C U ( N O ~ ) ~ - rates of Pb removal can be achieved when larger root mass is used. 3H20, Zn(N03)2.6H20,Ni(N03)2.6H20,and K2Cr207were T
TABLE 1
Heavy Metal Uptake by Roots of Brassica juncea concentration metal Zn Cd Cr Ni
cu Pb a
amount
solution (meRI
rootsa kg/g
solution
DW f SE)
(Ice)
100 2 4 10 6 2
13147 f 1815 268 f 41 716 f 30 1080 f 373 2943 f 261 1126 f 77
40000 800 1600 4000 2400 800
roots
(re
f SEI
18378 f 2903 440 f 15 815 f 49 1795 f 295 2339 f 147 806 f 5
recovety in roots ( O h f SE)
bioaccumulation coefficient
45.9 f 7.3 55.0 f 1.8 50.9 f 3.1 44.9 f 7.4 97.5 f 6.1 100.8 f 0.6
131 134 179 208 490 563
Roots were exposed to different metal solutions for 24 h (see Figure 6 ) f SE ( n = 3).
VOL. 29, NO. 5 , 1 9 9 5 / ENVIRONMENTAL SCIENCE &TECHNOLOGY
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Time (hours) FIGURE 4. (A) lead removal by live or dried roots of B. juncea from solutions initially containing 300 mg of PbR. (B)Pb content of dried and live roots after 96 h. Dried roots were prepered by placing excised roots at 80 "C for 24 h followed by washing in running water for 3 h and redrying at 80 "C. Dried roots and live roots dried at the end of the experiment weighed 0.5 f 0.1. Controls contained aerated PbZ+ solutions without plant roots. Vertical bars denote SE ( n = 4). TABLE 2
lead Accumulation in Roots of Different Plantsa commom name
scientific name
Pb in roots (mg/g DW f SE)
DicotyledonousCrops Indian mustard sunflower wild cabbage tobacco spinach
Brassica juncea (L.) Czern. Helianthus annuus L. Brassica oleracea L. Nicotiana tabacum L. Spinacia oleracea L.
we sorghum corn
Secale cereale L. Sorghum bicolor (L.) Moench Zea mays L.
colonial bent grass Kentucky bluegrass creeping bent grass weeping love grass perennial rye grass hard fescue sheep fescue rough bluegrass creeping red fescue tall fescue orchardgrass
Agrostis tenuis Sibth. Poa pratensis L. Agrostis palustris Huds. Eragrostis curvula (Schrad.) Nees. Lolium perenne L. Festuca ovina L. var. duriuscula (L.) Koch. Festuca ovina L. Poa trivialis L. Festuca rubra L. Festuca arundinacea Schreb. Dactylis glomerata L.
centipede grass buffalo grass switch grass coastal panic grass Bermudagrass Japanese lawngrass filter paper control
Eremochloa ophiuroides (Munro) Hack. Buchloe dactyloides (Nutt.) Engelm. Panicum virgatum L. Panicum amarum P.G. Palmer Cynodon dactylon (L.) Pers. Zoysia japonica Steud.
136 f 6 140 f 5 134 f 15 132 f 6 95 f 25
MonocotyledonousCrops
104 f 8 88 f 7 75 f 13
Cool Season Grasses
169% 1 1 165 f 16 146 f 3 142 f 12 134 f 3 125 f 7 111 f11 100 f 7 86 f 4 85 f 3 6 0 f 15
Warm Season Grasses
124 f 13 118f3 116f5 109 f 9 90 f 7 56 f 2 2f0
* Pb accumulated in the root tissue was measured after 3 days of exposure to 300 m g of Pb/L f SE ( n= 41.
At 35 and 70 mg of Pb/L, allthe metal removed from the solution in 72 h was absorbed by B. juncea roots (Figure 3). At higher concentrations, more Pb was removed from the solution than accumulated in the roots. This difference between Pb in roots and Pb removed from solution 1242
ENVIRONMENTAL SCIENCE &TECHNOLOGY / VOL. 29, NO. 5 , 1 9 9 5
increased as a function of metal concentration. Thus, total Pb disappearance from a solution initially containing 500 mg of Pb/L was four times greater than the amount of Pb accumulated in the roots and was equal to 45.1% of the root DW. This difference was accounted for by the
formation of an amorphous white precipitate on the walls and at the bottom of the hydroponic container. Infrared spectroscopic analysis of the precipitate identified lead phosphate as its major component. The Pb content of the roots was relatively independent of the Pb concentration in the solution, indicating that root adsorption saturated at 92-114 mg of Pblg DW of roots. Analysis of the Pb in roots treated with 300 mg of Pb/L for 24, 48, and 72 h showed a Pb content of 144.8 f 6.7, 172.0 f 6.2, and 119.4 f 9.2 mglg, respectively, indicating that the root Pb absorption is a rapid process which is completed in the first 24 h. At concentrations below 150 mg of PblL, plants did not show visible signs of toxicity for the duration of the experiment, while plants exposed to 300 and 500 mg of PblL showed reduction in growth and chlorosis. Only live roots were able to remove Pb effectively from water. After 96 h, live roots reduced the Pb concentration from 300 mg/L to below the detection limit of 0.1 mg/L or by at least 3000-fold (Figure4A). Over the same time period, dried roots produced only a 36%reduction in the initial Pb concentration. On a DW basis, live roots were 1.9 times more effective in absorbing Pb than dried roots, which were washed in deionized water before exposure to Pb (Figure 4B). This implies that live roots precipitated much greater amounts of Pb than dried roots. After 72 h, excised live roots immersed in aerated solution were only slightly less effective in removing Pb from water than live roots attached to the plants (data not shown). To determine the effect of different amounts of root mass on Pb removal from solution, different amounts of freshly excised B. junceu roots were immersed in 400 mL of 110 mg/L Pb solution for 72 h. The speed of Pb removal from the solution was directly proportional to the mass of the excised roots as long as some Pb remained in the solution at the end of the experiment (Figure 5A). However, since 0.78 g of roots removed all Pb from the solution in 72 h, further increase in root mass had no effect on Pb removal. As expected, the levels of Pb accumulated in root tissue during the experiment were not dependent on the root mass and remained at approximately 100 mglg DW (Figure 5B). Lead was not the only metal effectively removed from water by roots. This was demonstrated by immersingroots of hydroponically grown B. junceu plants in 400 mL of deionized water containingCd2+(2 mg/L), Ni2+(10 mglL), Cu2+(6 mglL), Zn2+(100 mglL), C P (4 mg/L), or Pb2+(2 mg/L) (Figure 6). These concentrations exceeded NJ groundwater quality criteria by 500-, 400-, loo-, 40-, 20-, or g-fold, respectively (17). Experimental plants did not show visible phytotoxicity for the duration of the experiment. In 8 h, roots dramatically reduced the content of all tested metals in solution. Bioaccumulation coefficients, the ratio of metal concentration in root tissue (uglg DW) to initial metal concentration in solution (mglL), determined after 24 h of metal treatment vaned significantly for different metals (Table 1). At the concentrations used, Pb had the greatest bioaccumulation coefficient of 563 while Zn had the lowest, 131. The bioaccumulation coefficients of metals were not proportional to the initial concentration of each metal in the solution. Significantly more Cd, Ni, Cu, Zn, and Cr were removed from solution than recovered in roots (Table 1). This suggests that these metals were not
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only absorbed by the roots but also precipitated from the solution by root exudates or possibly transported to the shoots. As already mentioned, Pb is also precipitated by roots. However, levels of Pb used in this experiment were below the levels at which precipitation normally occurs (seeFigure 3). Roots removed the chromium anion, Cr042-, almost as efficiently as the cations of other metals (Figure 6). X-ray absorbance spectroscopy analysis demonstrated that B. junceu roots exposed to a solution of C P contained mainly Cr3+,indicating that B. junceu roots can effectively reduce chromate (D. Salt, unpublished). The ability of B. junceu to accumulate Pb in roots was compared to that of 24 plant species that included four dicotyledonous (broadleaf)crops, three monocotyledonous (cereal) crops, and 17 cultivated grasses (Table 2). Grasses were tested because they can rapidly regenerate roots after pruning-a property which could be beneficial in a continuously operating rhizofiltration process. A filter paper control was used to demonstrate that Pb uptake was root specific. All tested species had a remarkable ability to concentrate Pb in the roots (17%on a DW basis for colonial bentgrass and 6% for Japanese lawngrass). B. junceu (14% Pb in dried roots) was among the best metal accumulators tested in the experiment. VOL. 29, NO. 5,1995 / ENVIRONMENTAL SCIENCE &TECHNOLOGY
1243
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FIGURE 6. Removal of different metals from aqueous solutions by B. juncea roots (0). Metal ions are indicated on the top of each panel. Metal concentrations in 10-mL aliquots removed from solutions were determined by DCP with a detection limit of 0.15 p@g. This value was assigned to all measurements below the detection limit. Control treatments (0)did not contain roots. Roots immersed in the solution had DW from 0.7 to 1.7 g. Vertical bars denote SE ( n = 4).
Discussion Our results indicate that the roots of terrestrial plants have an intrinsic ability to absorb and precipitate heavy metals from solutions. The amounts of metals accumulated in roots can exceed 10%of root DW. The nonlinear kinetics of metal disappearance observed over the range of solution concentrations suggest that plant roots utilize several mechanisms for metal removal. These mechanisms are not necessarily similar for different metals. In the case of Pb, absorptionby the root is probablythe fastest component of metal removal. Surface absorption is a combination of such physical and chemical processes as chelation, ion exchange, and chemical precipitation of metal ions. Biological processes are probably responsible for the slower components of metal removal from the solution. These biological processesinclude intracellular uptake and translocation to the shoots (14,181. Because metal transport to the shoot makes rhizofiltration less efficient by producing more contaminated plant residue, plants used for rhizo1244 9 ENVIRONMENTAL SCIENCE &TECHNOLOGY / VOL. 29, NO. 5, 1995
I
filtration should not be efficient translocators of metal. Fortunately, the ability of plants to translocate Pb to shoots varies much more than their ability to accumulate metals in roots (14). The third and slowest component of Pb removal, particularly pronounced at high metal concentrations, involves root-mediatedprecipitation of Pb from the solution in the form of insoluble lead phosphate. Most likely, this precipitation involves a release of root exudates. The combination of these processesproduces the characteristic nonlinear kinetics of Pb disappearance from solution (Figures 1, 4, and 6). The effectiveness of the removal process is such that live roots of B. junceu incubated in 500 mg/L Pb solution for 72 h removed an amount of Pb equivalent to 45% of their DW (Figure 3). Washed dried roots of B. junceuwere much less effective in removing Pb from solution (Figure 4). In contrast to live roots, dried roots exhibited only the rapid kinetic component, which may be explained by Pb interaction with
polygalacturonic acid and other negatively charged molecules within plant cell walls (19). The longer term components of Pb removal such as cellular uptake and precipitation require biological activity of living cells. Little is known about the mechanisms that allow plants to accumulate metals intracellularly or to export them to the shoot. The vacuole plays an important role in the storage of such metal ions as Cd (20). Inside the vacuole, metal ions are thought to be chelated by organic acids, such as citrate or malate, or by enzymatically synthesized (yEC)-isopeptidescommonly called phytochelatins (21). Organic acid complexes and other phytochelates may also be involved in long distance metal transport in plants (22). Continued studies of the mechanisms ofheavy metal uptake by root tissue should provide important insights that can increase the efficiency of rhizofiltration. Additional improvements in rhizofiltration may be achieved through better understanding the role of rhizosphere microorganisms in metal uptake and precipitation by roots. Other biological materials such as wool fiber and melon husks have been previously investigated for their metal remediating ability (23,241. However,these materials were at least 50-fold less effective in Pb removal than the live roots of B. junceu. In addition, B. junceu is a high biomass crop which, when grown hydroponically,can produce large amounts of roots rapidly and economically. The advantages of using roots for water treatment include the ability to treat a variety of metals at low concentrations and high water volumes without the use of toxic chemicals. Also, the high concentration of accumulated metal in roots will substantially reduce the amount of secondary waste. At the end of the rhizofiltrationprocess, metal-richplant roots are harvested and dried. Shoots can be discarded or allowed to regenerate new roots depending on the species used. Dried material may be combusted to further reduce its mass and to produce energy for the operation of the rhizofiltration system. Acids may be used to strip metals from the plant residue followed by reclamation of metal from the acid solution. Alternatively, metal-enriched plant material can be buried at the hazardous waste site. The use of roots of terrestrial plants to remove heavy metals from aqueous solutionsmay provide the foundation for a novel water treatment technology. Conceivably, rhizofiltrationmay be applicable to the treatment of surface water and groundwater, industrial and residential effluents, downwashes from power lines, storm waters, acid mine drainage, agricultural runoffs, diluted sludges, and radionuclide-contaminated solutions. The economic competitiveness of rhizofiltration has never been tested. However, this technology has time on its side since plants are one of the few renewable resources forever available to man.
Acknewldgwnts This work was supported by the U.S. Department of Environment (Grant R818619),New JerseyCommission for Science and Technology Grant 93-240380-1, New Jersey Agricultural Experiment Station,Phytotech Inc., and Exxon Co. We thank Alan Baker, David Salt, and Burt Ensley for helpful discussions. We also thank Roger C. Prince, Ingrid J. Pickering, Graham N. George, and Archana Supanekar for technical assistance. P.B.A.N.K., V.D., and I.R. have equity in Phytotech Inc., which commercializes the use of plants for environmental remediation.
Literature Cited (1) Janson, C. E.; Kenson, R. E.; Tucker L. H. Environ. Prog. 1982, 1, 212-216. (2) Moore, M. D.; Kaplan, S. ASM News 1994, 60, 17-23. (3) Summers, A. 0. Curr. Opin. Biotechnol. 1992, 3, 271-276. (4) Jackson,P. J.; Torres, A. P.; Delhaize, E.; Pack, E.; Bolender, S. L. J. Environ. Qual. 1990, 19, 644-648. (5) Tobin,J. M.; White, C.; Gadd, G. M. J. Ind. Microbiol. 1994,112, 126-130. (6) Sela, M.; Garty, J.; Tel-Or, E. New Phytol. 1989, 112, 7-12. (7) Kay, S. H.; Haller, W. T.; Garrard, L. A. Aquat. Toxicol. 1984, 5, 117-128. (8) Turnquist,T. D.; Urig, B. M.; Hardy, J. K. J. Enuiron. Sci. Health 1990, A25, 897-912. (9) Dierberg, F. E.; DeBusk,T. A.; Goulet, N. A., Jr. InAquaCicPlants for Water Treatment and ResourceRecoueT,Reddy, K. R., Smith, W. H., Eds.; Magnolia Publishing Inc.: Orlando, FL, 1987; pp 497-504. (10) Mo, S. C.; Choi, D. S.; Robinson, J. W. J. Environ. Sci. Health 1989, A24, 135-146. (11) Jain,S. K.;Vasudevan,P.; Jha,N. K. Biol. Wastes 1989,28, 115126. (12) Dittmer, H. J. Am. J, Bot. 1937, 24, 417-420. (13) Raskin, I.; Kumar, N.; Dushenkov S.; Salt, D. Curr. Opin. Biotechno2. 1994, 5, 285-290. (14) Kumar, P. B. A. N.; Dushenkov, S.; Motto, H; Raskin, 1. Environ. Sci. Technol. 1995,29, 1232-1238. (15) Baker, A. J. M.; Brooks, R. R. Biorecouery 1989, 1, 81-126. (16) Baker, A. J. M.; Reeves, R. D.; Hajar, A. S. M. New Phytol. 1994, 127, 61-68. (17) New JerseyAdministrative Code. Ground Water Quality Standards; 1993, 7, 9-6, 153-182. (18) Cataldo, D.A.;Wildung, R. E. Enuiron. HealthPerspect. 1978,27, 149-159. (19) Punz, W. F.; Sieghardt, H. Environ. Exp. Bot. 1993, 33,85-98. (20) Vogeli-Lange,R.; Wagner, G. J. Plant Physiol. 1990, 92, 10861093. (21) Rawer, W. E. Annu. Rev. Biochem. 1990, 59, 61-86. (22) Kinnersely, A. M. Plant Growth Re@. 1993, 12, 207-217. (231 Balkose,D.; Baltacioglu,H. J. Chem. Technol. Biotechnol. 1992, 54,393-397. (24) Okieimen, F. E.; Onyenkpa,V. U. Biol. Wastes 1989, 28, 11-16.
Received for review July 25, 1994. Revised manuscript received December 27, 1994. Accepted Janualy 12, 1995.@ ES9404750 @Abstractpublished in Advance ACSAbstracts, February 15,1995.
VOL. 29, NO. 5,1995 I ENVIRONMENTAL SCIENCE &TECHNOLOGY 1 1246
