Modeling the Plant Uptake of Organic Chemicals, Including the Soil

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Environ. Sci. Technol. 2010, 44, 998–1003

Modeling the Plant Uptake of Organic Chemicals, Including the Soil-Air-Plant Pathway C H R I S D . C O L L I N S * ,† A N D EILIS FINNEGAN‡ Soil Science Department, Reading University, Reading RG6 6AW, and Centre for Environmental Policy, Imperial College, London SW7 2AZ, United Kingdom

Received July 1, 2009. Revised manuscript received November 10, 2009. Accepted December 7, 2009.

The soil-air-plant pathway is potentially important in the vegetative accumulation of organic pollutants from contaminated soils. While a number of qualitative frameworks exist for the prediction of plant accumulation of organic chemicals by this pathway, there are few quantitative models that incorporate this pathway. The aim of the present study was to produce a model that included this pathway and could quantify its contribution to the total plant contamination for a range of organic pollutants. A new model was developed from three submodels for the processes controlling plant contamination via this pathway: aerial deposition, soil volatilization, and systemic translocation. Using the combined model, the soil-air-plant pathway was predicted to account for a significant proportion of the total shoot contamination for those compounds with log KOA > 9 and log KAW < -3. For those pollutants with log KOA < 9 and log KAW > -3 there was a higher deposition of pollutant via the soil-air-plant pathway than for those chemicals with log KOA > 9 and log KAW < -3, but this was an insignificant proportion of the total shoot contamination because of the higher mobility of these compounds via the soil-root-shoot pathway. The incorporation of the soil-air-plant pathway into the plant uptake model did not significantly improve the prediction of the contamination of vegetation from polluted soils when compared across a range of studies. This was a result of the high variability between the experimental studies where the bioconcentration factors varied by 2 orders of magnitude at an equivalent log KOA. One potential reason for this is the background air concentration of the pollutants under study. It was found background air concentrations would dominate those from soil volatilization in many situations unless there was a soil hot spot of contamination, i.e., >100 mg kg-1.

Introduction The uptake of organic pollutants by vegetation is an important component of the risk assessment when determining the suitability of areas contaminated with these chemicals for their future development or existing use. Plants may become contaminated by organic chemicals via a range of pathways. Several authors have hypothesized that the soil-air-plant * Corresponding author e-mail: [email protected]; phone: +44 (0)118 378 8910; fax: +44 (0)118 3786666. † Reading University. ‡ Imperial College. 998

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pathway is significant (1-5). This pathway arises when chemicals volatilize from the soil in which the crop is growing with subsequent aerial deposition to the plant. The soil-airplant pathway has not received as much attention as uptake via the roots or direct aerial deposition from the background air and more importantly has not been quantified for the range of chemicals of concern (6). Wang and Jones (7) reported that the concentrations of chlorobenzenes in carrot foliage grown on contaminated soils correlated with the KOA, suggesting that the soil-air-plant deposition pathway was dominant. Tao et al. (8) and Kipopolou et al. (9) also found significant aerial deposition to plants grown on contaminated soils. Smith et al. (10) proposed that soil outgassing of the lighter polycyclic aromatic hydrocarbons (PAHs) may be a significant pathway for the contamination of the overlying vegetation, while Trapp and Matthies (1) reported it would only be significant for high soil concentrations of TCDD. The soil-air-plant pathway is considered to be important because many compounds of concern are not readily transferred from the root to the shoot because of their high log KOW values. The accepted range for transpiration stream mobile chemicals is log KOW ) -1 to +5, but this is a bell distribution with a peak at log KOW ≈ 2 (11-13). More recent studies have proposed a sigmoidal relationship with higher transport of the chemicals with log KOW < 2 (14, 15). In their screening framework Ryan et al. (16) suggested that those chemicals with a dimensionless Henry’s law constant (KAW) of greater than 10-4 would contaminate vegetation predominantly by the soil-air-plant pathway. Duarte-Davidson and Jones (17) proposed a framework for the foliar uptake of chemicals volatilizing from soil following the application of sewage sludge: chemicals with a log KAW > -4 and log KOA > 9 would have high uptake via the soil-air-plant pathway, for those with log KAW > -4 or log KOA > 9 uptake would be medium/possible, and for those compounds with log KAW < -4 and log KOA < 9 uptake would be negligible. Cousins and Mackay (18) suggested that uptake from the atmosphere is the important pathway for chemicals with log KOA > 6 and log KAW > -6. Many persistent organic pollutants such as PAHs, PCBs, and PCDD/Fs are within the physicochemical boundaries outlined above and so can potentially accumulate via the soil-air-plant pathway. The aim of the present study was to determine the magnitude of the soil-air-plant pathway in relation to the total uptake of organic pollutants by vegetation from contaminated soils. This aim was divided into three objectives. (1) Determine the best method of modeling aerial deposition to vegetation by comparing the ability of three models with different approaches to predict the plant bioconcentration factor from a number of data sets. No widely accepted model for aerial deposition exists. (2) Combine the soil volatilization model of Johnson (19) and the soil to shoot transfer model of Trapp and Matthies (20), both of which are well recognized and have performed well in intercomparison studies (21, 22), and the best aerial deposition model from objective 1. Use this newly developed model to quantify the soil-air-plant pathway in relation to the total plant uptake of a range of frequently detected organic pollutants. (3) Assess the new model’s performance against a range of published data and determine under what conditions the soil-air-plant pathway would play a significant role.

Data Collection and Processing The data were collected from a number of studies (Table 1). These were chosen because they were in reviewed journals, 10.1021/es901941z

 2010 American Chemical Society

Published on Web 01/07/2010

TABLE 1. Citation and Short Description of Data Sets Used in This Study authors

contaminated matrix

Bacci et al. (25)

air

Hiatt (26)

air

Jones and Duarte-Davidson (27)

air

Smith et al. (10)

air

Scheunert et al. (28)

soil

Allard et al. (29)

soil

Samsoe-Petersen et al. (30)

soil

Wang and Jones (7)

soil

experimental description

chemicals used

crops were exposed to vapors of pesticides in an enclosed chamber containing plants in pots samples of ambient air and local vegetation taken vegetation samples taken from a range of sites and ambient air concentration measured over the growth period aerial deposition to an established sward monitored laboratory study with crops grown in soil contaminated with chlorobenzenes laboratory study using plant uptake of PAHs from a contaminated soil field study with crops grown in PAH-contaminated soils glasshouse study with crops grown in PAH-contaminated soils

were written by established researchers in the area, and/or provided good experimental detail, e.g., air and plant concentrations and a clear indication of how these had been derived. The chemicals used in these studies represented a wide range of KOA (log KOA ) 3-15) and KAW (log KAW ) -0.1 to -8.3) values and represented important classes of industrial pollutants. All bioconcentration factors (BCFs) were calculated assuming plant material is 80% water and has a density of 800 g kg-1; these are averages for a range of crops from a USDA database (23). Soil concentrations were expressed by dry weight. Air to vegetation (BCFAV) and soil to vegetation (BCFSV) bioconcentration factors were calculated as follows: BCFAV )

concentration in plant shoot (mg m-3 wet weight) concentration in air (mg m-3)

BCFSV )

concentration in plant shoot (mg kg-1 wet wt) concentration in soil (mg kg-1 dry wt)

Values for the octanol/water partition coefficient (KOW) and the dimensionless Henry’s law constant (KAW) for the pollutants under study were taken from the Syracuse Research Corp. Datalog database (http://www.syrres.com/esc/efdb.htm) or a recent review concerning the fate and transport of the PAHs, PCBs, and BTEX (24). The KOA was calculated from the division of KOW by KAW.

Modeling Comparison of Aerial Deposition Models. The plant contamination models under investigation had three different approaches to calculating the BCF. The model of Bacci et al. (25) is a simple regression model which relates the BCF to the KAW and KOW of the target chemical: log(BCFAV) ) -1.95 + 1.14 log KOW - log KAW

(1)

The model is referred to as BAC hereafter. The model of Riederer (31) is a partition model using fugacity theory that calculates the BCF on the basis of the

range of log KOA

pesticides

6.89-10.38

VOCs

3.30-5.05

PCDD/Fs

9.35-12.71

PAHs

6.59-11.50

chlorobenzenes

1.88-4.77

PAHs

6.59-12.97

PAHs

6.04-10.83

chlorobenzenes

4.41-6.75

partitioning of the chemical to different leaf components, e.g., lipids: BCFAV ) VA + VW/KAW + VCKCA + VGKGA

(2)

where VA ) volume fraction of air in the leaf (0.5), VW ) volume fraction of water in the leaf (0.4), KAW ) air to water partition coefficient ) dimensionless Henry’s law constant, VC ) volume fraction of cuticle in the leaf (0.01), KCA ) cuticle to air partition coefficient ≈ KOA, VG ) volume fraction of lipids in the leaf (0.001), and KGA ) cuticle to air partition coefficient ≈ KOA. The model default values are in parentheses. The model is referred to as RIED hereafter. The model of Trapp and Matthies (20) is a mechanistic model that considers air-leaf exchange, metabolism, and dilution by plant growth. A key property of the uptake process is the partition coefficient between the plant tissue and water, which is based on the lipid concentration in the plant. Deposition onto the shoot from the surrounding air is solved using a mass-balance approach. Growth dilution and metabolism within the plant compartment are calculated using first-order half-lives. Only growth dilution was used in the present study because reliable values for plant metabolism do not exist for the chemicals under investigation. dCleaf ) -RCleaf + β dt

(3)

where Cleaf ) concentration in the leaf tissue of the plant (mg m-3), R ) loss term (d-1), and β ) uptake term (mg m-3 d-1). The loss term comprises the diffusive transfer from the leaf to air and dilution by growth: R)

Aleafgleaf + Kplant growth KLAVleaf

(4)

where Aleaf ) leaf surface area (m2) (5), gleaf ) conductance (m d-1) (86.4), KLA ) leaf/air partition coefficient (dimensionless), Vleaf ) leaf volume (m3) (0.002), Kplant growth ) pseudofirst-order rate constant for dilution by plant growth (d-1) (0.035). The leaf surface area increases during growth, but the model theory is valid as long as the ratio of the leaf area to the leaf volume remains constant: KLA ) KLW/KAW VOL. 44, NO. 3, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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b )(FP/FW) KLW ) (WL + LLKOW

where WL ) plant compartment weight fraction of water, LL ) lipid fraction of plant compartment by weight (specific crop value from ref 21), b ) correction exponent to account for differences between plant lipids and octanol (0.97), FP ) density of the plant compartment (800 kg m-3), and FW ) density of water (1000 kg m-3). The uptake term of the differential equation calculates the gaseous uptake from air: β)

Aleaf C g Vleaf air leaf

(5)

where Aleaf ) leaf surface area (m2) (5), Cair ) air concentration (mg m-3), gleaf ) conductance (m d-1) (86.4), and Vleaf ) leaf volume (m3) (0.002). The steady-state concentration in the leaf from aerial deposition is now given by the ratio of the uptake and loss terms: Cleaf(∞) )

βair Rair

(6)

where Cleaf ) concentration in the leaf tissue (mg m-3). The model default values are in parentheses. The model is referred to as TMair hereafter. Quantification of the Contribution of the Soil-Air-Plant Pathway. Air concentrations resulting from soil volatilization were calculated using the methodology of Johnson et al. (19). This model was chosen because it had performed well in a previous model intercomparison (21) and it is used within several established risk assessment models (32, 33). The model assumes steady-state conditions have been attained between contaminants sorbed to soil surfaces and the airfilled pore space. Cair ) (VF)Csoil

(7)

FIGURE 1. Accumulation of organic contaminants in vegetation from experimental data (BCFAV ) bioconcentration factor of air to vegetation, KOA ) octanol/air partition coefficient): b, experimental data; O, BAC, Bacci model; 4, RIED, Riederer model; 0, TMair, Trapp and Matthies model. where Rsoil ) Kplant growth

(10)

βsoil ) Q(TSCF)(Cwater/Vleaf) where Q ) transpiration stream flux (m3 s-1) (1.15 × 10-8), TSCF ) the higher value from 0.784 exp[-(log KOW - 1.78)2/ 2.44] or 0.7 exp[-(log KOW - 3.07)2/2.78], Cwater ) concentration in soil water (mg m-3), Vleaf ) leaf volume (m3) (0.002), and Kplant growth ) pseudo-first-order rate constant for dilution by plant growth (d-1) (0.035). Cwater is calculated from the bulk soil concentration (Csoil): Cwater ) Csoil/Kd

(11)

-3

where Cair ) concentration in air (mg m ), Csoil ) concentration in soil (mg kg-1 dry wt), and VF ) volatilization factor (kg m-3) KAWF

VF ) [θwater

[

UairδairLs + KdF + KAWθair] + 1 + DeffW

]

× 103 (8)

where KAW ) air/water partition coefficient (dimensionless), F ) dry bulk density (g cm-3) (1.40), θwater ) water-filled soil porosity (cm3 cm-3) (0.25), Kd ) soil/water partition coefficient, θair ) air-filled soil porosity (cm3 cm-3) (0.25), Uair ) wind speed (cm s-1) (50), δair ) height of the ambient mixing zone (cm) (20), Ls ) depth below the ground to the contamination source, Deff ) effective diffusion coefficient (cm2 s-1), and W ) width of the contamination source (cm) (1500). The model default values are in parentheses. The model is referred to as VOL hereafter. The values chosen were for a small vegetable plot on a sandy loam soil with the reference concentration in the middle of the crop canopy (10 cm) and crops grown for a 90 day period. Shoot contamination via root uptake was predicted using the model of Trapp and Matthies (20), such that the loss term only included growth dilution and not volatilization. Inclusion of volatilization underpredicts uptake via the roots, because this is already accounted for when calculating the transpiration stream concentration factor (TSCF) which these workers use in their model (22). dCleaf ) -RsoilCleaf + βsoil dt 1000

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where Kd ) 10(0.72 log KOW + 0.49) fOC in which fOC ) fraction organic carbon in soil. The model default values are in parentheses. The model is referred to as ROOT hereafter. The final model RAM (root air model) that is used to investigate the contribution of the soil-air-plant pathway comprises the three submodels TMair, VOL, and ROOT and calculates root and aerial uptake. Validation of the RAM Model with Experimental Data and Determination of Conditions Where It Will Be Significant. The RAM model was validated against the data from those experiments given in Table 1 where the soil was the contaminated matrix. All data were converted to BCFSV to enable direct comparison with the model. The RAM model was then used to calculate the ambient air concentration for a soil contamination of 1 mg kg-1, the mean value for urban soils reported by the WHO (34). This value was compared with a range of literature values for urban and rural air concentrations to determine which source, soil or background air, has the greater significance for plant contamination.

Results and Discussion Comparison of Aerial Deposition Models. Two distinct phases for the relationship between BCFair and log KOA can be seen in the experimental results (Figure 1): an equilibrium phase for those compounds with log KOA between 3 and 8, followed by a plateau between log KOA ) 8 and log KOA ) 13. There does not appear to be a third increasing phase for BCFAIR where log KOA > 11 as a consequence of particle deposition as proposed by McLachlan (35). This indicates that in these studies gaseous deposition is the primary process contaminating vegetation. The data are therefore appropriate for testing the models under scrutiny. The linear predictions

FIGURE 2. Variation in the aerial deposition to the plant shoot with log KOA and log KAW of chemicals: O, experimental data. The contour map was created from a distance-weighted least-squares fit to the data. of the models BAC and RIED do not account for the plateau in the graph above log KOA ) 8. The model TMair also predicts a linear relationship for those chemicals for log KOA e 8; additionally it predicts the plateau in the BCFAV with log KOA > 8. This plateau arises because the model accounts for the influence of growth dilution. McLachlan (35) proposed that the deposition of organic pollutants with log KOA ) >7 is kinetically limited; i.e., the plant biomass is accumulating faster than it can attain equilibrium with the low concentrations of the pollutants in the atmosphere. The r2 values for the experimental versus predicted BCFAV for three models were 0.69, 0.56, and 0.90 for BAC, RIED, and TMair, respectively. On the basis of these findings, the model TMair was chosen to predict aerial deposition. Quantification of the Contribution of the Soil-AirPlant Pathway. Using the RAM model which combines the three submodels TMair, VOL, and ROOT, the total mass accumulated in the plant shoot as a result of aerial deposition and root uptake from a 1 mg kg-1 soil concentration of the contaminants under investigation was determined. The highest mass transfer via the soil-air-plant pathway was for those compounds with log KAW > -2 and log KOA < 6 (Figure 2). However, only those compounds with log KOA > 8 and log KAW < -3 transferred greater than 10% of their total accumulation via the soil-air-plant pathway, with the maximum being 36% for indeno(1,2,3-c,d)pyrene (log KOA ) 10.8 and log KAW ) -4.18) (Figure 3). Hexachlorobenzene (log KOA ) 6.75 and log KAW ) -1.20) was an exception to this rule, transferring 10.3% of the total uptake mass via the soil-air-plant pathway. The findings are in agreement with those of Cousins and Mackay (18) and further qualify DuarteDavidson and Jones’s (17) framework that only those chemicals with log KAW > -4 and/or log KOA > 9 would have significant uptake via the soil-air-plant pathway. A number of chemicals of concern such as the carcinogenic PAHs, PCDD/Fs, higher chlorinated PCBs, and flame retardants are within these chemical boundaries. The results demonstrate the advantage of modeling over screening frameworks because a range of outcomes can be seen and the pathways of importance for individual pollutants can be readily quantified. Validation of the RAM Model with Experimental Data and Determination of Conditions where It Will Be Significant. When compared to experimental data, the RAM model predicted a steady decline in the BCFSV where log KOA > 4 and < 7, followed by a plateau where KOA > 7; this was also the general trend of the data (Figure 4). Where KOA > 7, the contamination via the soil-air-plant pathway is relatively

FIGURE 3. Variation in the fraction of the total deposition arising from soil volatilization and subsequent deposition to the plant shoot with log KOA and log KOW: O, experimental data. The contour map was created from a distance-weighted least-squares fit to the data.

FIGURE 4. Variation in the log bioconcentration factor of soil to vegetation (BCFSV) with log KOA of chemicals for experimental and modeled data: experimental data from Scheunert et al. ([), Allard et al. (9), Samsoe-Petersen et al. (b), and Wang and Jones (2); RAM (root air model) (0). stable (Figure 3). Additionally, uptake via the root is kinetically limited because of the low soil solution concentration of these compounds as a consequence of their high affinity for soil carbon. Hexachlorobenzene exhibited higher plant accumulation than expected from the overall trend in the experimental data in two studies as it had done in the modeling study (Figure 3). The BCFSV of the experimental data was highly variable with up to 2 orders of magnitude difference between data sets at equivalent log KOA. SamsoePetersen (30) recognized that their BCFSV values were lower than those other studies, but they could find no obvious reasons for such variability. Potential confounding factors are the differing scales of the studies, e.g., laboratory, glasshouse, or field, and/or the soil contamination procedure; soils in some experiments were spiked while others used field soils where the pollutants had aged. Pollutants are known to become more sequestered in soils as they age and hence less available for plant uptake (36, 37). There is a paucity of plant uptake studies in the literature where all the factors, e.g., plant species, soil type, and contaminant age, are comparable to provide a less variable data set. The variability in the literature data made a test of the model difficult, but it predicted the overall trend in the data (r2 ) 0.51). However, because of the data variability, the RAM model was not a major improvement of the ROOT model (r2 ) 0.53), which does not include the soil-air-plant pathway. VOL. 44, NO. 3, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 2. Modeled and Measured Air Concentrations of PAHs with Potential To Contaminate Plants via the Soil-Air-Plant Pathway

PAH benz[a]anthracene chrysene benzo[b]fluoranthene benzo[a]pyrene benzo(g,h,i)perylene indeno(1,2,3-c,d)pyrene dibenz(a,h)anthracene a

calcd air reported reported concn for gas-phase gas-phase -1 a 1 mg kg air concn, air concn, (ng m-3) urban (ng m-3) rural (ng m-3) 0.19 0.04 0.009 0.005 0.001 0.002 0.002

0.16-0.97 0.21-1.58 NDb to 0.28 ND to 0.06 ND to 0.02 ND to 0.02 ND

Values derived from the RAM model.

b

ND to 0.01 0.05-0.148 ND to 0.153 ND to 0.1 ND to 0.12 ND to 0.06 ND

Not detected.

Using the RAM model, air concentrations were derived using a typical urban soil contamination level of 1 mg kg-1 (32) for those PAHs that fulfill the criteria where deposition via the soil-air-plant pathway is >10% of the total uptake, i.e., log KAW < -3 and log KOA > 8 (Table 2). The RAM model calculated air concentrations were lower than reported concentrations for many urban and rural locations (9, 38-43). These findings indicate that only in areas of high soil concentrations (10-100 mg kg-1) is deposition to crops via the soil-air pathway likely to be greater than that from the background air. These findings are supported by field experiments for a range of pollutants including PCBs, HCH, DDT, PCDD/Fs, and PAHs (8, 9, 44, 45). It is difficult to compare the deposition from the soil-air-plant pathway with contamination arising from particle transport via resuspended soil. For chemicals with high KOA (>11) particulate deposition is likely to dominate the background deposition (35), but particulate mass loadings from resuspended soil vary widely from 0.26 g g-1 (46) to 0.0002 g g-1 (47). Which value is chosen will profoundly affect the magnitude of deposition via this pathway.

Supporting Information Available Descriptions of the models used in this study. This material is available free of charge via the Internet at http:// pubs.acs.org.

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