Environ. Sci. Technol. 2007, 41, 6704-6710
Competitive Uptake of Trichloroethene and 1,1,1-Trichloroethane by Eucalyptus camaldulensis Seedlings and Wood E . R . G R A B E R , * ,† A . S O R E K , † L. TSECHANSKY,† AND N. ATZMON‡ Institute of Soil, Water and Environmental Sciences, The Volcani Center, Agricultural Research Organization, P.O.B. 6, Bet Dagan 50250 Israel, and Institute of Plant Sciences, The Volcani Center, Agricultural Research Organization, P.O.B. 6, Bet Dagan 50250 Israel
The efficient use of trees for taking up volatile organic compounds (VOCs) from the subsurface for remedial and screening purposes is hampered because many poorly quantified co-occurring processes affect VOC concentrations in the tree, the most basic of which are VOC sorption and uptake by roots. Toward understanding the dominant sorption mechanisms, uptake of trichloroethene (TCE) and 1,1,1-trichloroethane (TCA) by Eucalyptus camaldulensis seedlings was studied in both single-solute and bi-solute experiments. Single-solute and bi-solute sorption experiments on wood from a mature Eucalyptus camaldulensis specimen were also carried out. Competition between TCE and TCA for sorption sites was found in both seedling uptake and wood sorption experiments, indicating that partitioning is not the sole mechanism governing compound interactions in these systems. The nonlinear singlesolute sorption isotherms on wood were fit by a dualmode model including partitioning and Langmuir terms. The dual-mode model calculated parameters were consistent with the results of the bi-solute sorption experiments. As a consequence of competitive sorption processes, uptake of individual compounds may be lower than expected when multiple VOC contaminants are present in the subsurface.
Introduction Volatile organic compounds (VOCs), including chlorinated solvents such as trichloroethene, tetrachloroethene, and dichloroethene isomers, are very common pollutants in subsurface environments. Many resources are expended in efforts to detect and clean up such pollutants in the subsurface, as even small amounts can cause widespread contamination of groundwater and the unsaturated zone. In recent years, the ability of trees and other plants to take up VOCs from the subsurface via the transpiration stream has been exploited for both remediation (phytoremediation) and subsurface screening purposes (phytoscreening, or phytomonitoring). Several studies have suggested that VOCs measured in vegetation can be used to estimate subsurface concentrations, both of groundwater and of the gas phase * Corresponding author e-mail:
[email protected]. † Institute of Soil, Water and Environmental Sciences. ‡ Institute of Plant Sciences. 6704
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of the vadose zone (1-5). The estimation ability is only qualitative, as many different poorly quantified processes occur in tandem and affect VOC concentrations in the tree. These processes include VOC uptake by roots and their transfer into the transpiration stream (6, 7), upward transport in the xylem (8, 9), diffusion both into the tree stem and out to the atmosphere (10-12), sorption onto the woody tissues of the tree (1, 13-17), and compound transformations inside the tree (3, 18, 19). Basic understanding of these mechanisms and their interactions in the subsurface-tree-atmosphere continuum, along with obtaining good estimates for the dominant parameters, is essential for the goal of quantifying the relationship between VOC concentrations in the tree and in the subsurface. VOC uptake by the root and compound movement into the xylem cells of the root are perhaps the most fundamental of these many processes, as they are a prerequisite for all the others. By and large, the uptake of anthropogenic organic chemicals by plant roots has been shown to be a passive process, consisting of establishment of sorption equilibrium between compounds inside the plant root and compounds in the aqueous or gas phases of the surrounding medium (6, 7, 20). Studies which focused on developing predictive relationships for organic chemical uptake based upon compound physical-chemical properties generally reported a maximum in transpiration stream concentration factor (TSCF; the ratio of apparent concentration in the xylem to the concentration in the external solution) as a function of compound octanolwater distribution coefficient (Kow) (6, 8, 21, 22). The maximum TSCF (between 0.7 and 0.8) occurs at a compound log Kow value ranging from about 1.8 to 3, depending on the correlation used (7), with the correlation for environmentally important VOC compounds peaking at a log Kow of about 2.5 (21). While the mechanisms responsible for such a maximum are not fully understood, it has been suggested that more hydrophilic compounds are less capable of crossing lipid membranes in the root, while more lipophilic chemicals are strongly retained in the root lipids and other sorbing structures in the root, and do not pass readily into the transpiration stream (7). Considering that reported relationships are based on data measured at one level of external solution concentration, the implicit assumption is that the TSCF is independent of external solution concentration. A tacit part of this assumption is that the presence of multiple organic solutes does not have an impact on uptake of the individual solute into the roots. The independence of individual solute distribution coefficients in multiple solute systems is a feature of equilibrium partition processes (23). Sorption and uptake of non-ionic compounds or the neutral form of ionic compounds by plants has been frequently treated as a partitioning process, based largely on observed linear relationships between compound concentration in the water phase and in the biomass in sorption experiments (13, 14, 24-27). Few studies have actually tested the relationship between VOC concentration in the external solution and in the plant via plant uptake experiments (1, 18). In one experiment, the ratio of 14C-labeled TCE in carrots, spinach, and tomatoes to the initial dose level was similar (within statistical error) at 2 initial aqueous concentrations (18). In another, a linear relationship between TCE concentration in rooted poplar cuttings and in a hydroponics solution was reported (1). Inasmuch as partitioning is explicitly or implicitly considered to be the dominant mechanism governing VOC sorption in plants, virtually all studies have explored VOC 10.1021/es070743l CCC: $37.00
2007 American Chemical Society Published on Web 09/05/2007
uptake and sorption in single-solute systems despite the fact that at many contaminated sites where phytoremediation or phytoscreening techniques are applied, the subsurface is contaminated with a mixture of VOC contaminants. The purpose of the present contribution was to explicitly test the partitioning mechanism by comparing uptake of trichloroethene (TCE) and 1,1,1-trichloroethane (TCA) by Eucalyptus camaldulensis seedlings over a range of aqueous phase concentrations, in both single-solute and bi-solute systems. Complementary single-solute and bi-solute sorption experiments on Eucalyptus camaldulensis wood were also conducted. TCE and TCA were chosen as they are common VOC contaminants, are frequently found together in the same contaminated environment, and have similar physicalchemical properties (Table S-1 in the Supporting Information). With such experiments, it is possible to gain insights into the mechanism of VOC uptake and sorption by woody plant material, as well as an improved understanding of the utility of phytoscreening or phytomonitoring for estimating subsurface VOC concentrations.
Materials and Methods Sorption Experiments. A branch about 10 cm in diameter was removed from a thriving Eucalyptus camaldulensis tree and air-dried for about 3 months. After removing the bark, the branch was ground to pass through a 2 mm sieve and additionally dried at 50 °C for several days. Sorption experiments (23 ( 2 °C) were carried out in 10 mL vials equipped with Teflon-lined septa and crimp hole caps at a ratio of 1:10 wood/aqueous solution of 0.03 M CaCl2 + 1.0 mM NaN3 (to suppress microbial activity) (0.5 g wood/5 mL solution). After soaking the wood in aqueous solution for 24 h, the vials were cooled on ice and appropriate amounts of stock solution of TCE (Merck, AR) and TCA (BioLab, AR) prepared in methanol (MeOH) or neat were added to the solutions in each vial, and the vials were quickly sealed. Maximal added amount of MeOH was 0.2%, which is not expected to affect sorption of the target compounds (28). Blank vials and calibration standards were prepared identically, with glass beads in place of the wood as to maintain equal headspace volumes in sample, blank, and calibration vials. The solid/liquid ratio afforded about 40% sorption compared with blank vials. Sorption kinetics (3 replicates, 3 blanks) was tested over the course of 10 days. TCA equilibrium was reached within 2 days, and TCE equilibrium was reached within 6 days; therefore, all equilibrium experiments were carried out for 6 days, using 3-4 replicate samples and blanks at each concentration point. Vials were shaken on a table shaker for the duration of the sorption experiment. As in refs 29-31, analysis was carried out by analyzing the headspace at room temperature of each vial and comparing it to an equal volume of headspace of external calibration aqueous standards, also at room temperature. Knowing the initial amount added and the volume of liquid and gas phases, aqueous and gas-phase concentrations were calculated using Henry’s coefficients. Sorbed amount was then determined by difference in aqueous concentration between nominal aqueous concentration without sorbent and with sorbent. Results were not corrected for blank losses, which averaged below 3%. TCE and TCA concentrations were determined by gas chromatography (GC) using a flame ionization detector (FID; automated Varian 3800 instrument, CA) and automatic headspace sampler (CTC Analytics, Switzerland). For bi-solute experiments, stock solutions of both TCE and TCA together were prepared in ratios such that the initial concentration of the competitor in the experimental vials was fixed, while the initial concentration of the other compound was varied. The effect of a fixed initial amount of TCA on sorption of TCE, and of fixed initial amount of TCE on sorption of TCA, was tested.
Seedling Uptake Experiments. Eucalyptus camaldulensis seeds were germinated in germinating trays containing vermiculite in a temperature-controlled greenhouse (22 °C). After about 1 month, the seedlings were transferred to 330 mL growing containers in a medium composed of vermiculite/peat/styrofoam at 20:20:60 ratio. At 3 months of age, the substrate was soaked in water for several hours and then gently rinsed from the roots, and seedlings were placed in an aerated 0.25 Hoagland nutrient solution for 3 days. For the flow-through uptake experiment, a 10 L Tedlar bag was filled with deionized water and the bag was shaken gently for 24 h by shaker table, after which any air bubbles that accumulated were extruded (usually no more than about 2 mL in volume). The neat VOC compound was injected inside the bag to give the desired solution concentration, and the bag was returned to the table shaker for 48 h. Before the experiment was begun, Hoaglands nutrient solution was injected inside the Tedlar bag to bring the nutrient concentration to 0.1 Hoaglands, and the bag was shaken for another hour. The nutrient solution was maintained at a relatively low concentration to minimize possible development of microorganisms. The specially designed flow-through chamber consisted of a hollow glass cell (15.5 × 15.5 × 5.5 cm) with eight holes of 14 mm diameter drilled in the top. These holes were for the seedlings, which were introduced via a fitted Teflon plug with a slit along one side for the stem. The stem was wrapped with Teflon tape along the portion in contact with the plug, and the slit was also wrapped with Teflon tape. The roots were inside the chamber, while the stem and leaves were outside. For introducing the test solution into the chamber, a 0.7 cm diameter hole was drilled 1 cm above the bottom of the chamber, and for solution exit, a 0.7 mm hole was drilled 1 cm from the top of the chamber. A 1 cm layer of airspace was maintained in the chamber so as to avoid oxygen stress to the seedlings. The chamber was shielded with Al foil to avoid exposing the roots to light. After filling the flow cell to within 1 cm of the top with the appropriate Hoaglands and VOC solution and sealing the top holes with 7 seedlings in Teflon plugs, and an eighth plug without any holes (used as a sampling port), the nutrient-VOC solution from the prepared Tedlar bag was pumped through the chamber at a rate of 1 mL/min by peristaltic pump. The peristaltic pump and Tedlar bag system made it possible to pump VOCcontaining solution from the bag through the chamber without introducing any air. This is essential in experiments with VOCs, as their concentration in solution changes as the volume of air in the system changes. The chamber solution concentration was sampled via the sampling port for VOC analysis throughout the course of the uptake experiments. Two parallel chambers were fed simultaneously from the same Tedlar bag, and each sample included 7 seedlings. The experiments were conducted in a fume hood under constant lighting by two 60 W plant bulbs (Osram, Augsburg, Germany) at 20-23 °C. Five experimental series were performed: (1) uptake kinetics of TCA at different concentrations; (2) equilibrium uptake experiments of TCA between 2 and 58 mg/L; (3) equilibrium uptake experiments of TCE between 4 and 47 mg/L; (4) equilibrium uptake experiments of TCA (4-47 mg/ L) in the presence of TCE at about 134 mg/L; and (5) equilibrium uptake experiments of TCE (2-33 mg/L) in the presence of TCA at about 120 mg/L. Seedlings were removed from the chamber after the specified time, and the roots were quickly dipped in deionized water and blotted on absorbing paper. Roots, leaves, and stems were separately ground in liquid nitrogen and added to 10 mL headspace vials prepared with 5 mL of 500 mg/L NaN3 which were quickly sealed. The plant material from each of the replicate seedlings was homogenized to VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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average out natural differences between individual seedlings. The extent of VOC differences between individual seedlings can be seen in Figure S-1 (Supporting Information). The test substances were extracted from the plant material by heated headspace (95 °C for 20 min, including agitation), and the headspace was analyzed by GC-FID. Neither TCE nor TCA were recovered in the leaf portions, thus only roots and stems were analyzed for the majority of the experiments. Extraction efficiency was tested by spiking ground wood and extracting it 6 days later using the same heated headspace technique. Extraction efficiency for TCA was 98% ( 4% and for TCE was 93% ( 4%; results are not adjusted for this. TCA uptake kinetics was tested at intervals of 24, 48, 96, and 144 h. Results show that no changes in measured concentrations were recorded after 48 h (Figure S-2 in the Supporting Information). As such, equilibrium uptake experiments were conducted for 48 h. These results mean that steady state was reached among all the mechanisms possibly affecting VOC concentrations in the system (translocation, sorption, volatilization, degradation) within the time given for the seedling uptake experiment. Contaminant Toxicity Test. With the flow-through system, it was not possible to measure seedling transpiration rates for testing the possible effect of toxicity of the contaminants. Therefore, an additional experiment was conducted under batch conditions, whereby seedlings were exposed to different levels of TCE and TCA, and water uptake was measured per unit of foliage dry mass. Three treatment levels were tested simultaneously with 7 replicate seedlings per treatment: (i) 70 mg/L TCE + 150 mg/L TCA in 0.1 Hoaglands; (ii) 60 mg/L TCA + 150 mg/L TCE in 0.1 Hoaglands; and (iii) 0.1 Hoaglands (control). Treatments (i) and (ii) represent concentrations greater than the highest concentrations of contaminants in the flow-through uptake experiments. Experiments were conduced in 40 mL glass vials equipped with Teflon-lined silicone septa and screw caps. The stem of the seedlings above the root mass was introduced into a slit septum and sealed there with Teflon tape. The slit was sealed with a special Teflon tape that binds to Teflon. The root mass was introduced into 40 mL glass vials pre-prepared with 0.1 Hoaglands solution and the appropriate amounts of contaminant filled to zero headspace, and the vials were sealed. The seedlings were then exposed for 48 h to the same lighting and temperature conditions as in the flow-through experiments. After this time, the aboveseptum leaf biomass was removed, dried at 65 °C for 2 days, and weighed. With the root mass still intact inside the vial, water was added to fill each vial, and the weight of the added water was determined. Water uptake is given as g H2O/dry leaf mass in mg.
Results and Discussion Wood Sorption. Results of single-solute and bi-solute sorption experiments on wood are depicted in Figure 1A and B for TCA and TCE, respectively. The single solute isotherms of both compounds are nonlinear, and can be described by the Freundlich model (S ) KfCn, where S is sorbed concentration at equilibrium, C is solution concentration at equilibrium, Kf is the Freundlich coefficient, and n is the Freundlich exponent; parameters in Table 1). The TCE isotherm exhibits greater nonlinearity (n ) 0.77 ( 0.02) than the TCA isotherm (n ) 0.86 ( 0.02). Sorption in the bi-solute experiments is reduced as compared with that in the singlesolute experiments (see Figure 1 inset graphs for greater detail), indicative of competitive sorption processes. Bi-solute isotherms are well described by the linear Henry’s model (S ) KdC; where Kd is the distribution coefficient calculated as the slope of the best-fit linear regression with zero intercept; Table 1). 6706
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To achieve a more in-depth mechanistic understanding of the nonlinear sorption in this system, the single-solute isotherms were additionally treated by a dual-mode model involving a partitioning domain and an adsorption domain:
S ) KdC +
CbQ 1 + bC
(1)
where the first term on the right-hand side of the equation represents the partitioning domain (Henry’s), and the second term represents the adsorption domain (Langmuir model). In the second term, b is the sorption affinity and Q is the capacity of Langmuir sites. By applying the dual-mode model, we envision wood to consist of two sorption domains: a partitioning domain characterized by a linear isotherm, and an adsorption domain characterized by a nonlinear isotherm with a maximum capacity (Q) for sorption as a result of a limited number of sorption sites for interaction. The dualmode model is widely used for describing sorption in varied systems, including polymers, soil organic matter, and wood (15, 32-34). The dual-mode conception can be tested as in this work, by applying a competitor at a high concentration which will occupy all the limited Langmuir sites. The second solute can then occupy only the partitioning mode. If the dual-mode model is appropriate, the measured Kd in the bi-solute experiment should give the same Kd as calculated via eq 1 for the partitioning mode in the single-solute experiment. While the dual-mode model returned similar Kd values for both compounds (5.61 ( 0.31 L/kg for TCA and 5.38 ( 0.73 L/kg for TCE), the Langmuir capacity for TCE was about twice the Langmuir capacity for TCA (1559 ( 721 L/kg versus 798 ( 351 L/kg, respectively). For TCA, the dual-mode model returned an estimated distribution coefficient of the partitioning term that was quite close to the Kd value actually measured in the bi-solute experiment (5.61 ( 0.31 L/kg compared with 6.29 ( 0.19 L/kg; Table 1; Figure 1). The corresponding TCE Kd value for the partitioning domain alone was rather lower (by about 30%) than the experimental value in the bi-solute experiment (5.38 ( 0.73 L/kg versus 7.73 ( 0.16 L/kg; Table 1; Figure 1). These results accord with the experimental conditions applied in the respective bi-solute experiments, and with the results from the single-solute experiments. Considering the TCA bi-solute experiment, the initial fixed concentration of the TCE competitor (588 mg/L) corresponds to an equilibrium solution concentration of 246 mg/L in the single-solute TCE experiment. Via the dual-mode model fitting of the TCE isotherm, it can be calculated that at this equilibrium solution concentration, sorbed TCE is distributed at a concentration of 959 mg/kg in the Langmuir domain and 1323 mg/kg in the partitioning domain. In other words, the TCE competitor dominates the nonlinear domain available to TCA in the bi-solute experiment (estimated by the dual-mode model to be 798 ( 351 mg/kg); therefore, the partitioning-mode Kd and measured Kd in the bi-solute experiment correspond well. For the TCE bi-solute experiment, the initial fixed concentration of the competitor TCA at 544 mg/L corresponds to an equilibrium concentration of 221 mg/L, with sorbed TCA distributed, according to the dual model fitting, between 476 mg/kg to the Langmuir domain and 1240 mg/kg to the partitioning domain. As such, TCA does not occlude all available TCE Langmuir sites (1559 ( 721 mg/kg), and TCE in the bi-solute isotherm can access both partitioning and Langmuir domains. Therefore, the measured TCE bi-solute Kd is rather larger than the partitioning-mode only Kd. The success of the dual-mode model in interpreting the results of the bi-solute experiments lends support to the validity of the dual-mode mechanism of sorption in the studied system. A similar dual-mode mechanism was invoked by Severtson and Banerjee (15) for sorption of chlorophenols on wood pulp.
FIGURE 1. Aqueous sorption on Eucalyptus wood of (A) 1,1,1-trichloroethane (TCA) and (B) trichloroethene (TCE). Markers denote average of replicates, and error bars denote standard deviation of the replicates. Inset graphs are an enlargement of the low concentration region. The dual-mode model fit of the single solute isotherms is shown by a solid line; the linear model fit of the bi-solute isotherms is shown by a dashed line. Also shown on the figure and labeled are the separate Langmuir and partitioning modes of the dual-mode model for the single-solute isotherms. The ratio of distribution coefficient of the Langmuir expected to have the most pronounced effect on sorption of domain (Qb) to the distribution coefficient of the partitioning the second solute when the second solute is present at domain (Kd) is twice as large for TCE (1.88) as for TCA (0.95), relatively lower aqueous concentrations (i.e., the range where denoting the relative dominance of the site-specific Langmuir the Langmuir domain is coequal or dominates the partitiondomain for TCE as compared with TCA. This can also be ing domain). The sorption affinity and capacity for the seen graphically in Figure 1, where the TCE site-specific Langmuir domain of the competing compound will deterLangmuir domain is more important than the partitioning mine at which concentration it will affect sorption of a second domain at concentrations below 134 mg/kg, whereas for TCA, component. the two domains are co-equal at concentrations below 50 Seedling Uptake Experiments. Results of the seedling mg/L. Therefore, when a competitor is present at concenuptake experiments in both root and stem compartments trations sufficiently high to occlude the Langmuir sites, it is are depicted in Figure 2. Uptake is best described by a simple VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Fit Parameters for Linear, Freundlich, and Dual-Mode Models for Wood Sorption Experimentsa linear system TCA-single TCA-bisolute TCE-single TCE-bisolute
Freundlich
Kd L/kg
R2
6.29 ( 0.19
0.989
7.73 ( 0.16
0.995
dual mode
Kf (mg/kg)(mg/L)n
n
R2
16.0 ( 1.9 7.77 ( 2.70 32.85 ( 4.33 4.99 ( 1.08
0.86 ( 0.02 0.960 ( 0.007 0.77 ( 0.02 1.08 ( 0.05
0.998 0.990 0.998 0.996
Kd L/kg
b L/mg
Q mg/kg
R2
5.61 ( 0.31
0.0067 ( 0.0044
798 ( 351
0.998
5.38 ( 0.73
0.0065 ( 0.0038
1559 ( 721
0.998
a K of the linear model is calculated as the slope of the least-squares linear regression with zero intercept. Other model parameters are calculated d using a nonlinear curve fitting procedure. Intervals represent the standard error of parameter estimate.
FIGURE 2. Single- and bi-solute uptake results on root and stem portions of Eucalyptus seedlings. The slope (Kd, L/kg), standard error of the slope, and R2 of the regression are indicated in the figure for single-solute (‘single’) and bi-solute (‘bi’) experiments. linear correlation with external concentration for most of the experiments, with the possible exception of the bi-solute experiment with TCE in the presence of TCA for the stem fraction (Figure 2B). Kd, the Henry’s distribution coefficient, is calculated as the slope of the best-fit linear regression with zero intercept (Figure 2). The experimental variability in the seedling uptake experiments is greater than that in the wood sorption experiments, as the seedling uptake experiments are more difficult to control and additionally suffer from natural variability between the seedlings (Figure S-1, Supporting Information). Despite the relatively large scatter, it is seen that distribution coefficients in the bi-solute seedling uptake experiments are reduced in the presence of the competing compound in all cases (Figure 2). The substantially lower distribution coefficients in the stem compartment as compared with the root compartment (Figure 2) reflect the equilibrium achieved between upward translocation from the roots through the stem and into the leaves, and dissipation from the system via evapotranspiration from the stem and leaves. Uptake experiments were carried out over a much 6708
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smaller range of concentrations than the wood sorption experiments to avoid metabolic stress to the seedlings. As a result, saturation of sorption sites in the single-solute uptake experiments was not observed. Despite the linear relationships, however, competition for the specific sorption domain with a fixed number of sites is apparent in the results (Figure 2). The phytotoxicity experiments designed to test seedling metabolic stress showed that water uptake by the seedlings in the batch systems (in units of g of water per mg of dry leaf mass) was the same for the three treatments: (i) TCA dominated, 0.013 ( 0.004 g/mg; (ii) TCE dominated, 0.014 ( 0.004 g/mg; (iii) control, 0.015 ( 0.009 g/mg. Thus it can be concluded that in the uptake experiments there was no contaminant toxicity and that uptake reduction in the presence of two contaminants was the result of competition for sorption sites. Nature of the Non-Linear Sorption Domain. Although sorption and uptake of non-ionic compounds or the neutral form of ionic compounds by plants has frequently been
treated as a partitioning process (13, 14, 24-27), the results presented in Figures 1 and 2 demonstrate the presence of a limited sorption domain in addition to a partitioning domain. A limited sorption domain can result in a nonlinear relationship between internal and external solution concentration, and also in competition between coexisting solutes for sorption sites. Though the current bi-solute experiments for VOC seedling uptake and wood sorption are apparently unique, there is other evidence in the literature for both nonlinear and linear VOC uptake by wood in single-solute experiments. Ma and Burken (1) conducted air-biomass and water-wood sorption experiments for TCE, tetrachloroethene (PCE), and carbon tetrachloride (CCl4) individually on poplar wood (Populus deltoids x P. nigra). Linear sorption isotherms were obtained for TCE and CCl4 both for gasphase and aqueous-phase experiments, while PCE isotherms were fit by a linear regression with a nonzero intercept, and thus are actually nonlinear. In a later work, aqueous PCEpoplar wood sorption data was also fitted with a linear isotherm with a nonzero intercept (2), thus demonstrating nonlinear sorption behavior. In both studies, PCE isotherms were convex to the x-axis, possibly indicating pore-filling or condensation in pores, multilayer sorption, or sorbent swelling. In sorption experiments by Mackay and Gschwend (13) on Ponderosa pine and Douglas fir, isotherms for benzene and toluene were found to be linear. The isotherm of o-xylene on Pondersosa pine was also linear, but for the fir, the intercept was again nonzero. In this case, the isotherm was concave to the x-axis. Severtson and Banerjee (14) reported linear isotherms for 2,4-dichlorophenol and 2,4,5trichlorophenol in processed wood fiber over a narrow low concentration range, but observed concave nonlinear isotherms and competitive sorption behavior over a wide concentration range (15). Such behavior has also been observed in the current study for TCE and TCA, as epitomized by the results in Figure 1. The results reported here are relevant for woody plants, where lignin is the major sorbent of organic contaminants (13, 25). Lignin makes up about 25-35% of wood content depending on the species, with the lignin content of mature Eucalyptus camaldulensis wood varying between 29 and 32% (35). While no information was available in the literature for lignin content of Eucalyptus seedlings, the lignin content of stems of 4 month-old dogwood (Cornus stolonifera) seedlings was reported to be about 20% (36). Like for wood, both linear and nonlinear sorption behavior has been reported for lignin. Xing et al. (24) reported linear sorption isotherms for benzene, toluene, and o-xylene on organosolv and alkali lignin, and nonlinear sorption of phenol on organosolv lignin (25). Other studies showed nonlinear sorption isotherms for various organic compounds on different lignin preparations: isoproturon on hydrolytic lignin (37); chlorophenols on Kraft lignin (15); and phenanthrene (34, 38) and naphthalene (34) on organosolv lignin. Lignin, being a glassy polymer (dry glass transition temperature, Tg ∼ 150 °C) (15), may be expected to demonstrate nonlinear and competitive sorption behavior at temperatures below the glass transition temperature due to the presence of microporous holes, or voids, which are part of the internal glassy polymer matrix. A recent study summarizing the glass transition behavior of Kraft lignin concluded that its hydrated glass transition temperature is about 60 °C (33). It should be recalled that Kraft lignin (prepared with NaOH and Na2S at high T), organosolv lignin (organic solvent-derived), and hydrolytic lignin (strong acid hydrolysis) have all undergone harsh and chemically altering isolation procedures, such that the resultant materials may have very different sorption and thermal characteristics from each other and from that of intact lignin in wood. However, if unaltered lignin has thermal and sorptive behavior similar to that of these lignin extracts, then at environmentally
relevant temperatures, nonlinear and competitive sorption behavior in the glassy lignin could be anticipated. In addition to being a glassy biopolymer, lignin has significant hydrogen bonding ability, deriving from its aliphatic hydroxyl groups and dimeric biphenyl-type structure (39). These additional site-specific sorption domains will be compound specific both in terms of sorption affinity and capacity. It can be speculated that the reason for the greater TCE Langmuir domain capacity (Q) and the greater relative dominance of the Langmuir domain over the partitioning domain as compared with TCA is due to the hydrogen bonding ability of TCE (40). In contrast, TCA has no or little such potential for hydrogen bonding (40). The dual-mode model returned the same Kd for both TCE and TCA (Table 1), suggesting that the two compounds have similar interactions in the linear partitioning domain, as could be predicted on the basis of their similar log Kow and aqueous solubility values (Table S-1, Supporting Information). Considering the glassy nature of the lignin polymer as well as its ability to undergo hydrogen bonding via different types of moieties, it is clear that the Langmuir term in the dual-mode model (eq 1) unavoidably represents more than a single limited sorption domain. This is why the Langmuir capacity (Q) returned for TCA (nonspecific sorption in the glassy voids) is smaller than the Q for TCE (nonspecific sorption in glassy voids plus H-bonding). Results of this work show that in the studied systems, the measured single solute Kd can overestimate by up to a factor of 2, the actual sorption of that solute when the second competing compound is present. The relative dominance of the site-specific Langmuir domain will differ for different compounds as a function of the compound’s affinity for the Langmuir domain(s). For example, the Qb/Kd ratio for 2,4,5trichlorophenol (TCP) on wood fiber (15) can be calculated to be 2.84, demonstrating that for TCP, the Langmuir domain is yet more dominant than it is for TCE (Qb/Kd ) 1.88) or TCA (Qb/Kd ) 0.95). 2,4,5-TCP specific interactions in wood fiber were attributed in part to its hydrogen bonding ability (15), which can be expected to be stronger than that of TCE. Thus, the relative effect of neglecting competition between compounds occurring in mixtures could potentially become quite significant, depending on the specific system involved and the concentrations of components in the mixture. The nonlinear relationship between external solution concentration and sorbed concentration (Figure 1), as well as competitive uptake (Figure 2), suggests that the predictive relationships developed for compounds as a function of log Kow based on single-point transpiration stream concentration factors (TSCFs) may be oversimplified. For woody plants, the TSCF should probably be considered concentrationdependent. This may be one reason for the relatively large data scatter reported in TSCF-log Kow relationships (6, 8, 21, 22). Furthermore, as seen here, it should be assumed that single-solute TSCFs are not necessarily relevant for situations where there are multiple contaminants. Given that competition between coexisting solutes for sorption sites in woody plants can result in lower-than-predicted uptake of a given compound, it is clear that their use for quantifying the level of subsurface contaminants in areas contaminated with multiple VOC pollutants may suffer an additional level of uncertainty. The extent of uncertainty resulting from competitive sorption processes as compared with uncertainties due to variability in VOC levels spatially and temporally in a single tree, between different specimens of the same tree species, or between different species, still needs to be addressed.
Acknowledgments This research was supported by the Office of the Chief Scientist, Israel Ministry of Environmental Quality. VOL. 41, NO. 19, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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Supporting Information Available Table of relevant properties of the study compounds; figures showing TCA concentrations in individual seedling stems (Figure S-1) and the results of the seedling kinetics experiments (Figure S-2). This material is available free of charge via the Internet at http://pubs.acs.org.
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Received for review March 28, 2007. Revised manuscript received July 7, 2007. Accepted July 23, 2007. ES070743L
