Generic One-Compartment Model for Uptake of Organic Chemicals by

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Generic One-Compartment Model for Uptake of Organic Chemicals by Foliar Vegetation STEFAN TRAPP’ AND

leaves, metabolism and degradation processes, dilution by exponential growth. Partition Coefficients for Plant Tissue. The partition coefficient describes the concentration ratio between two neighboring phases in thermodynamic equilibrium and is a key property for the fate of compounds in the soil-plantair system. For plant tissue, it can be calculated from (4, 9)

MICHAEL MATTHIES Institute of Environmental Systems Research, University of Osnabriick, 0-49069 Osnabriick, Germany

A differential mass-balance equation for the uptake of organic chemicals into the aerial plant compartment from soil and air is derived. Processes considered are uptake from soil, gaseous deposition, volatilization from leaves, transformation and degradation, and growth. An analytical solution is developed. Chemical data needed are KOW,KAW,and reaction rate constants. Constant average values for environmental parameters are assumed. Plant properties are typical for grass and green fodder. Calculations for 2,3,7,8-TCDD, and the comparison to a recentlytested numerical four-compartment model shows the applicability of the mass-balance approach. The equation could be incorporated into existing multimedia and soil transport models and may be useful for the hazard assessment of contaminated soils.

Purpose Uptake of chemicals into vegetation is a major pathway for toxic substances into the food chain leading to human beings. Vegetation may also play a significant role in the mass balance of chemicals in terrestrial systems (1). Multimedia models (21, which are widely used and recommended for risk assessment of new and existing chemicals (31, do not include vegetation. Modeling of plant contamination processes, in particular for organic chemicals, is of growing interest. Models for the calculation of the uptake have been developed (5-8). However, for the purpose of risk assessment, these approaches may be too sophisticated. Here, we strictly simplify an existing model. This gives a ‘one-compartment-model’consisting of one equation for the calculation of uptake into above-ground plants. The equation requires the same chemical input parameters as those used in multimedia models, namely, KOW, KAW, and reaction rate constants. We also give estimates of average parameter values for environmental conditions. Two example calculations are carried out in detail.

Processes Processes considered are the following: translocation to shoots, gaseous deposition on leaves, volatilization from * E-mail address: [email protected],uni-osnabrueck.de; Fax: 541 969 2599.

0013-936X/95/0929-2333$09.00/0

!E 1995 American Chemical Society

49

where KpWis the partition coefficient between plant tissue and water (kg of substance/m3of p1ant:kg of substance/m3 of water), WP and Lp are the water and lipid content of the plant tissue (g/g),e p and gw are the densities of plant tissue and water (kg/m3),and b is a correction exponent for differencesbetween plant lipids and octanol. The exponent b for cut bean roots and stems was found to be 0.75 (9);for mazerated barley roots it was 0.77 (10). For barleyshoots, 0.95 was found (111,and for isolated citrus cuticles, it was 0.97 (12). Uptake from Soil into Roots. For fine roots, diffusive exchange with the soil is high, and near-equilibrium conditions are assumed to be achieved. For thicker roots, equilibrium is an upper limit, and the kinetics of uptake control the concentration. The partition coefficient between roots and bulk soil KRBis

where Kd is the distribution coefficient between soil matrix and water (L/kg),@B is the bulk soil density (here in kglL), and 8 is the volumetric water fraction of the soil. KRWis the partition coefficient between roots and water (mass/ volume to mass/volume), calculated analogously to eq 1. Values of eq 2 are close to 1 and only slightly depend on lipophilicity when Kd is calculated from KOCusing the method of Schwarzenbach and Westall (13). A plausible reason for the similar sorption properties of roots and soil is that the humic substances in soil originate from plant material. Measurements by E. M. Topp for barley and cress roots indeed support this finding (see ref 4 ) . Schroll and Scheunert (14)found KRWvalues of hexachlorobenzene for maize, oat, rape, and barley of between 0.8 and 3.2 but foundhigher values for lettuce (13.7)and carrot (31.6). Wang and Jones (15)found that the concentration ratio between carrot and soil of 10 chlorobenzenes varied also with the type of application. However, none of the KRWvalues (BCF fresh weight) were above 5; most of them were much lower. Their experiments also showed that concentrations in peels were always higher than those in cores, indicating the slow uptake kinetics into the tap root. From all this, it might be concluded that it is sufficient to assume that the concentration in fine roots is usually in or below the order of magnitude of the concentration in soil. Translocation with transpiration stream. The ‘transpiration stream concentration factor’ (TSCF)is defined as the concentration ratio between xylem sap and external solution (soil water). The mass transport within thexylem

VOL. 29, NO. 9, 1995 / ENVIRONMENTAL SCIENCE &TECHNOLOGY

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NxY(kgls) is then NV = QGTSCF

(3)

where Q is the transpiration stream (m3/s), Cw is the concentration in soil water, with CWsx CB/Kd, and CBis the concentration in (dry) bulk soil. The TSCF is related to the Kow (10):

TSCF = 0.784 exp[-(log KO, - 1.78)’/2.441 (4a) Hsu et al. (16) found an equation of similar form, but they gave different values: TSCF = 0.7 exp[-(log KO, - 3.07)’/2.781

(4b)

For substances with intermediate KOW,the equations work satisfactorily (compare, e.g., refs 17, 4, and 9). But from the comparison of both empirical equations, it can be seen that TSCF is an uncertain parameter, in particular for very lipophilic substances. In the following, the higher result from eqs 4a and 4b will be used. From theoretical considerations, it follows that TSCF values of nondissociating compounds should maximally be 1. Exchange with Air. Gaseous Exchange between Leaves anddtmosphere. The partition coefficient between leaves and air KLAis

KlA = KLWIKelW

(5)

where KAWis the partition coefficient between air and water (dimensionless Henry’s law constant) and KLWis the partition coefficient between leaves and water (dimensionless),calculated from eq 1. The coefficient bin eq 1is likely to be plant specific. We use experimental data from barley shoots ( b = 0.95) (11). When only the ‘bioconcentration factor’ in a partition model is required (equilibrium model), KIA is sufficient. Note that equilibrium might not be reached within one growth period for higher Kuvalues. When the mass balance is required, the flux must be calculated. The diffusive net flux between leaves and atmosphere (gaseous dry deposition) N), (kgls) is

NA = Ag[CA- C, / KU]

(6)

where A is the leaf surface area (m2),g is the conductance (mls),CAis the gas-phase concentration in air (kg/m3),and CL is the concentration in leaves (kg/m3). Estimates of average values for the conductance g (mls) are as follows: Lower boundary: cuticle is comparatively impermeable; uptake mainly via stomata [vapors, approximate when log KoW- log KAW< 5 (1811;conductance g is approximately 0.001-0.0001 mls, depending on plant species and environmental conditions. Upper boundary: cuticle is relatively permeable [verylipophilic compounds, approximate when log KO~V - log KAW> 10 (1811;the main resistance is from the atmospheric boundary layer, g is approximately0.005 mls (19). A default value ofg= 0.001 m/s is assumed. Amore detailed description is given in ref 18.

Dry Particulate and Wet Deposition. From the Junge equation follows the equilibrium distribution between particle bound and gaseous fractions (20). Substances with a vapor pressure of about Pa (20 “C) are half sorbed and half gaseous under typical background conditions. The gaseous and the particulate deposition have to be weighted 2334 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29. NO. 9.1995

with the corresponding fraction. Fine particulates (0.1- 1 ,urn)that are mainly responsiblefor the long-rangetransport of atmospheric particle-bound pollutants behave similar to gases but have lower deposition velocities (typically 0.1 mmls for 0.5 ,um diameter particles). They are also poorly scavenged (21). When particles are deposited on leaf surfaces and concentrations in both are in equilibrium, no diffusive net fluxof chemicalwill occur, although the particles present on the leaves carry an additional mass of compound. Wet deposition of gases is very effective for soluble substances, but on the other hand, the cuticle provides a very effective barrier for those chemicals. Both particle and droplet deposition may lead to a surplus flux, but the effect is only significant for low volatile organic chemicalswith negligible gas-phase concentrations. It was experimentallyconfirmed that, for manylipophilicand even for super lipophilic chloroorganics (DDT, HCB, PCB, PCDDlF up to hexaCDDlF),gaseous deposition is responsible for the contamination of grass and pine needles under outdoor (summer) conditions (22, 23). Subsequently, we do not include wet and particulate deposition in the equation. Note that the uptake predicted for vapor-phase processes alone is the minimum one (18). Metabolism and Photodegradation. Metabolism and photodegradation rate constants and l p are not calculated but must be supplied from experiments, literature, or external estimation routines. Plant metabolism differs from that of animals since no excretion organ exists and bound residues are often formed (24). Photodegradation is likely to occur since leaves are exposed to sunlight. Pseudofirst-order kinetics are assumed for the calculations. The sum of all rate constants is used:

AE = AM

+ Ap

(7)

where AE (d-’) is the elimination rate constant, composed of the metabolism rate constant and the photodegradation rate constant lp. Growth. The growth of plants depends on the stage of development. Shortly after germination, the growth is small. Then the vegetative phase follows where the main growth occurs. Finally, during the maturation stage, the growth comes to an end. During the vegetative phase, the growth can be approximatedby an exponentialfunction (2.3, and the dilution by growth can be calculated by a growth rate constant l~ (d-l) (26):

A, = In (Vend/VO)/t

(8)

where Vo and Vend are the volumes (m3)at the beginning and at the end of time period t (d). During the exponential growth, the ratio between leaf area andvolume (ANL),and subsequently between transpiration and volume (Q/VL),is relatively constant (26). This fact will be of use for the analytical solution (see below).

Deriving Equation for Uptake into Plants Mass Balance. The mass balance is change of chemicals mass in the aerial plant parts = flux from soil via xylem to the shoots Nxy (eq 3 ) f gaseous flux fromlto air NA (eq 6 ) photodegradation - metabolism (eq 7 ) .

+

Expressed in mathematical terms, it is

Input Data Bromacil (Data from ref 6); for Additional Data See Table 2 2.02 3-65 x 10-9 0.385 3250 dpm 0.0825 31.9-48.3 9.66 x 10-5 7.3 mUh = 2 x 9 0.046

log Kow KAW rate constant, AM CW(soil solution) (dpm) leaf area (in2) mass (g) volume (m3) transpiration duration of experiment (d) growth rate constant, 1~ (d- ’I

m3/s

Example Calculation convert all units to SI (m, kg, s)except chemical concn in dpm/mL concn in soil solution, CW:

C, = 3250 dpm/mL = 3.25 x IO9 dpm/m3 (3)

partition coefficient leaves to atmosphere, KLA:

KLw = (W,

+ LpKowb)e&w

+ 0.02 x (102.02)0.95) x 1/2 = 1.23

= {0.8

KLA= KLw/KAw= 1.23/3.65 x 19-’ = 3.37 x IO’

(4)

calculation of TSCF:

TSCF = 0.784 expi42.02 - 1.78)*/2.441= 0.77 TSCF = 0.7 exp[-(2.02

(5)

- 3.07)2/2.781= 0.47

higher TSCF is 0.77 uptake term b; from soil and air

b = b1

+ b2 = Q TSCF(&/VL) + gA(CA/VL)

uptake from soil b,:

b, = (2 x IO-’ m3/s x 0.77 x 3.25 x IO9 dpm/m3)/9.66 x

m3

= 5.18 x IO4 dpm s-l m-3 = 4.48 x IO9 dpm d-’ m-3

b, = uptake from air is zero (CA= 0) total uptake term b = bl = 5.18 x IO4 dpm sink term a (s-l): a = Ag/(K,VL)

s-l

m-3

+ 1, + 2,

= a,

+ a2

a1 is loss by volatilization from leaves to air:

m/s)/(3.37 x IO’ x 9.66 x

a, = (0.0825 m2 x

m3)= 2.5 x IO-’s-l

a2 is loss by metabolism plus dilution by growth: a, = 0.385 d-’

a = a, (7)

+ 0.046 d-’

+ a2 = 5 x

= 0.431 d-’ = 5 x

s-l (main sink is metabolism)

time to reach steady state (95%):

t(95%) = -In 0.05/a = 3.015 x

(8)

s-,

s-l = 6.9 d

steady state (95%) reached within 9 d, concn calcd from eq 13:

CL(-) = b/a = 5.18 x IO4 dpm s-l K 3 / 5 x =

s-l

10.36 x IO9 dpm W3= 20 720 dpm/g (wet weight)

+

dmL/dt= d(CLVL)/dt = Q TSCF C, &(CA - CL/KLJ - k m ~ (9) , where m~and VL are mass and volume of the leaves (m3). When growth is exponential and the ratios ANLand Q/VL are assumed to be constant, then it follows for the change

of the concentration with time (dCLldt) that d C L / d t = -[Ag/(KuVJ

+ & + &lCL + C,TSCF(Q/VL) + C&4/VL)

(10)

Analytical Solution for Constant Conditions. Taking the parameters on the right side of eq 9 as constants yields VOL. 29, NO. 9,1995 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

2335

a linear differential equation of first order:

TABLE 2

Input Data Environment (Normalized to 1 m2) where u = A~/(KLAVL) + dE + AG (sink terms) and b = CwTSCF(Q/Vd CA~(ANL) (source terms). With a given CL(0)the analytic solution of the equation is

+

The steady-state concentration (t

-

m,

dCL/dt

- 0) is

The time to reach steady state (95%) is t(95%) = -In 0.05/a

(14)

Limitations. The complex dynamic behavior of a chemical in the soil-plant-air system is reduced to one equation. This implies limitations. The approach is developed for nonionic organic substances; for the extension to dissociating chemicals, see ref 27. Fertilizers and inorganic dissociating compounds are taken up by plant transport systems, their behavior is different. There is no spatial differentiation of the plant. Calculated concentrations correspond to the aerial plant compartment, mainly foliage. Concentrations in fruits could be largely deviating. Exponential growth is assumed. This is only valid for plants that are harvested before maturation, e.g., green fodder, green vegetables, and lettuce. Transport of chemicals within the phloem is usually much smaller than within the xylem, but for chemicals with specificproperties (e.g.,some dissociating chemicals), it becomes very important (28). The deposition by aerosols could be included. But it is not clear whether it contributes significantly to accumulation from air, and at present it is not considered. The soilair-plant path that is of significance for volatile and semivolatile lipophilic chemicals needs a different solution (29). The empiric parameters used in this equation (Km, TSCF) are derived from a small number of experiments. The TSCF of nitrobenzene for seven plant species differed less than 10% (17)and was close to the results of eqs 4a and 4b. But for chemicals with high log KO", no experimental data are available. The given parametrization is not for a specific plant but represents average values. Moreover, properties are taken as constant. This is comfortable for the mathematical solution of the equation but is not very realistic and can lead to some error. It becomes clear from these limitations (the reader may find more) that the equation is of a generic type and less applicable for real situations where complex numerical models might be advantageous.

Calculations Two calculations are made to demonstrate the use of the equation. To allow the reader to follow the calculations, they are shown line by line. Comparison to Numerical Model PLANTX Experiments on the uptake of 14C-labeledbromacil (CsH13BrN202) into soybean plants (Glycine ma.)have recently been used to test a four-compartment numerical model (PLANTX) (6).We use the data of the BROM5 HT experiment to compare the outcome of eq 12 with those results. Input data are given in Table 1. 2330 1 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 9, 1995

shoot mass (kg) shoot volume, V ( m 3 ) leaf area, A (m2) lipid content, LP (g/g) water content, WP(g/g) transpiration, 0 time to harvest (d) growth rate constant, LG(d-') soil organic carbon content, oc (%) bulk soil density, @E (kg/L)

1 (26) 0.002 5 (26)

0.02 0.8 1 L/d = 1.15 x 60 (26) 0.035 (26)

m3/s

1

1.3

A direct comparison to the experimental results is not possible since metabolites were not calculated and concentrations in fruits, stem, and leaves are not given explicitly. The average bromacil concentration in aerial soybean parts, calculated with PLANTX [(6)Table 21, was very similar (20 331 dpm/g). The PLANTX model allows varying input and plant properties, growth, and phloem flux and calculates concentrations in roots, stem, leaves, and fruits. The strict simplification of the complex model to eq 12 does not give an incorrect result but less information. Application for Uptake of 2,3,7,8-TCDD. Dioxins and related compounds are now reassessed for their risk (see, e.g. ref 30). A major source for 2,3,7,8-TCDDis the uptake by food, e.g., milk and meat. Grazing animals take up PCDD/Ffrom the plants they eat (31). But howdoes2,3,7,8TCDD enter the plants? The followingcalculation addresses this question. Input data for the calculation are given in Tables 2 and 3. Plant and soil values are typical for a meadow. Some values were taken from a radionuclide model (26). They are normalized to 1 m2. The concentrations of 2,3,7,8-TCDDin soil and air are from measurements at a rural site (32). A laboratory experiment was carried out for the determination of the photodegradation of 2,3,7,8TCDD (33). The resulting rate constant ,IP (Table 3) is multiplied by 0.3 (30%of the time in full sunlight). It is not clear whether this rate constant is valid for environmental conditions. In an additional sensitivity analysis, Ap is set at zero. From the calculation, it can be concluded that for background conditions the uptake of 2,3,7,8-TCDDinto foliage is from air. (Even when the uncertain TSCF is set to its maximum, TSCF = 1, uptake from air is the major source.) This was confirmed by three investigations (36). Field experiments in Hohenheim, Southwest Germany (37, 38),showed a small dependency of leaf concentrations from soil concentrations, even on soils highly contaminated with PCDD/F, when a contamination by soil particles could be excluded. This holds for grass, corn, and nearly all vegetables. The only exceptions found until now are Cucurbituceu sp. (39).Calculated 2,3,7,8-TCDDconcentrations in plants are close to those measured in grass at Bayreuth (32),30-50 pg/kg dry weight, which is 6-10 pg/ kg wet weight, and to those from a rural site at Rothamstad, GB (32 pg/kg dry weight) (40).

ConcIusions By rigorous simplification of a recently tested fourcompartment plant uptake model, a single equation for uptake into the aerial plant compartment is derived. The principal structure includes uptake from soil, uptake from air, loss to air, dilution by growth, and loss by transforma-

TABLE 3

Input Data of 2,3,7,8=TCDD ref

6.76 6.374 0.0015 0.3744 d-’ 70 pg/kg 2.7 fg/m3

log Kow log Koc KAW rate constant, LP CB (dry soil matrix) CA (air, gaseous)

34 calcd from ref 35

34 33 32 32

Example Calculation convert all units to SI (m, kg, s)except chemical mass: 1000 fg = 1 pg = concn in soil solution, CW:

kg

C, % C$K, = C$(OCKo,) = 70 pg/kg/(O.Ol x 2 365 058 Ukg) = 0.003 pg/L = 3 pg/m3 (3)

partition coefficient leaves to atmosphere, KLA: KLW = (Wp

+ LpKowb)edew= (0.8 + 0.02 x (I06.76)0’95] x 1/2 = 26 424

KU = KLw/KAw = 26 424/0.0015 = 1.76 x lo7

(4)

calculation of TSCF: TSCF = 0.784 exp[-(6.76 - 1.78)2/2.44]= 3.0 x TSCF = 0.7 exp[-(6.76 - 3.07)2/2.78]= 5.2 x

(5)

higher TSCF is 5.2 x uptake term b = QTSCF(CW/VL) ~A(CA/VL) uptake from soil b1:

+

b, = (1.15 x lo-@m3/s x 5.2 x =9 x

IO-’ pg s-l

x

= 7.7 x

3 pg/m3)/0.002 m3 pg d-’ m-3

uptake from air, gaseous b2:

m s-l x 2.7 fg/m3)/0.002 m3

b, = Ag(CA/VL)= (5 m2 x = 6.75 fg

s-l

m-3 = 583 pg d-’ K3

total uptake term b is:

b = b,

+ b2 = 6.75 x

pg s-l m-3 = 583 pg d-’ rn-3(mainly from air)

+

+

sink term a = Ag/(KLAVL) + L E LG = a, a2 a1 is loss by volatilization from leaves to air:

a, = 5 m2 x

sf1

rn s-l/(1.76 x lo7 x 0.002 m3)= 1.4 x

a2 is loss by photodegradation plus dilution:

a, = 0.3744 d-’ x 0.30 a = a,

+ 0.035 d-’

+ a2 = 1.84 x

= 1.7 x

s-l

s-l

time to reach steady state:

t(95%) = -In 0.05/a = 3/1.84 x

s-’ = 1.63 x lo6 s = 19 d

steady state reached within 60 d, concn calcd from eq 13

CL(=) = b/a = (6.75 x =

pg s-l 1 ~ - ~ ) / 1 . x8 4

s-l

3.67 x lo3 pg m-3 = 7.3 pg/kg (wet wt)

sensitivity analysis: calculation without photodegradation loss term a = 5.45 x 10-7s-1

t(95%) = -In 0.05/a = 3/5.45 x

s-l = 63.7 d

C L ( 4= b/a = 6.75 x loW3pg s-l r1-~/5.45x

s-l

= 12.4 x IO3 pg m-3 = 24.8 pg/kg (wet wt)

C,(SO d) = b/a(l - e-&’

86400) = 23.3 pg/kg

(wet wt)

VOL. 29, NO. 9.1995 / ENVIRONMENTAL SCIENCE &TECHNOLOGY m

2337

tion. The substance data needed are not difficult to obtain except for degradation and metabolism rate constants. The computing effort is minimal, allowing a coupling to soil transport or multimedia models. Simple regressions with only one parameter (41,42) are only valid for specific situations and are of limited use. In contrast, the parameters for the proposed equation can be selected more specifically,e.g., contamination can be from air or soil. So it can be adapted to different scenarios. This makes this equation superior to regressions. The results are of a more generic type but gain some insight into dynamic behavior. The structure and parametrization is a suggestion for discussion. Partition coefficients, TSCF, and transfer velocities could be replaced by more plant-specific values. There are approximately 250 000 higher plants and more than a 1000 environmentally suspect chemicals. It cannot be expected that the approach will always work correctly. But hopefully, the equation can give some advice about the main processes, e.g., about the main uptake and sink process. This is helpful for the design and interpretation of measurements.

Acknowledgments Many thanks to Andreas Kaune for supplying us with literature.

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Received f o r review January 9, 1995. Revised manuscript received May 17, 1995. Accepted M a y 25, 1995.@

ES950008M Abstract published in Advance ACS Abstracts, July 1, 1995.