Organic Pollutant Accumulation in Vegetation STACI L. S I M O N I C H ’ A N D R O N A L D A. H I T E S * School of Public and Environmental Affairs and Department of Chemistry, Indiana University, Bloomington, Indiana 4 7405
Recent advances in the study of organic pollutant accumulation in vegetation are reviewed. Major areas include (a) the mechanism of uptake by vegetation, (b) the use of vegetation to indicate contamination levels, and (c) the importance of vegetation as a pollutant sink. The mechanism of vegetation uptake of organic pollutants is governed by the chemical and physical properties of the pollutant, environmental conditions, and the plant species. W e recommend that additional field studies be done on the uptake of industrial pollutants by native plants and that empirical models and controlled exposure experiments be validated under field conditions. Vegetation can be used to qualitatively indicate organic pollutant atmospheric contamination levels as long as the mechanism of accumulation is considered. Vegetation has been used to identify point sources of pollutants and to determine regional and global contamination patterns. Plant pollutant concentrations should be normalized to the plant lipid concentration or surface area, especially when directly comparing different species. Although vegetation has a great potential to accumulate organic pollutants, little is known about the quantitative importance of vegetation as a pollutant sink. Overall recommendations for future research are presented.
Introduction About 9 x lo8 kg of industrial organic pollutants were emitted into the United States’ atmosphere in 1989 ( I , 2). In addition, the United States uses about 4 x lo8 kg of organic pesticides every year (1, 3). Given the load of all these compounds to the environment, their possible persistence, and their possible health effects, it is important to understand their fate. Thus, scientists have studied the environmental fate of these compounds in sediment, soil, * E-mail address:
[email protected]. Current address: The Procter & Gamble Company, Environmental Science Department, 5299 Spring Grove Ave., Cincinnati, OH 45217+
1087.
0013-936X/95/0929-2905$09.00/0
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air, and water for many years. Only in the mid 1980s did substantial attention turn to vegetation (4). In the last 5-7 years, major advances in the study of the accumulation of organic pollutants by vegetation have been made by researchers throughout the world. This review focuses on these advances and suggests future directions for research in this field. Phytoremediation of organic contamination is not covered by this review; it is covered elsewhere (5). Recent studies on the accumulation of organic pollutants by vegetation can be dividedinto the following three areas: (a) the mechanism of uptake by vegetation, (b) the use of vegetation as a qualitative indicator of contaminant levels, and (c) the importance of vegetation as a pollutant sink. A significant amount of work has been done on the first two areas, but little work has been done on the last.
Mechanism of Uptake by Vegetation There are several pathways through which organic pollutants enter vegetation; these are shown in Figure l. The pollutant may enter the plant by partitioning from contaminated soil to the roots and be translocated in the plant by the xylem. (The xylem transports water from the roots to the leaves by transpiration.) Organic pollutants may also enter vegetation from the atmosphere by gas-phase and particle-phase deposition onto the waxy cuticle of the leaves or by uptake through the stomata and be translocated by the phloem. (The phloem transports photosynthatates to the roots and to other plant tissues.) These pathways are a function of (a) the chemical and physical properties of the pollutant, such as its lipophilicity, water solubility,vapor pressure (which controls the vaporparticle partitioning), and Henry’s law constant; (b) environmental conditions, such as ambient temperature and the organic content of the soil; and (c) the plant species, which controls the surface area and lipids available for accumulation. Figure 1represents a simplification of these pathways; in reality,vast differences exist between different plant species. These pathways have been investigatedusing empirical models (6-1 3 ,controlled exposure experiments in greenhouses or growth chambers (18-341, and field experiments (35-41). Soil to Plant. As shown in Figure 1, the extent to which an organic pollutant enters a plant’s roots from contaminated soil depends on the compound’s water solubility, Henry’s law constant, and octanol-water partition coef-
VOL. 29, NO. 12, 1995 /ENVIRONMENTAL SCIENCE & TECHNOLOGY
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if
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NIP, KO,, SA, lipids)
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FIGURE 1. Simplified mechanism of pollutant uptake by vegetation. The mechanism is a function of the following: WP(vapor-particle partitioning),IC,a(octanol-air partition coefficient), SA (plant surface area), lipids (plant lipid concentration), (octanol-water partition coefficient), solw (water solubility), H (Henry's law constant), orgo (organic content of the soil), and plant species.
ficient Wow) (6, 24). Other factors include the organic content of the soil and the plant species (6, 36). Hydrophilic Compounds. Uptake from soil through a plant's roots is the predominant pathway of accumulation for organic compounds that have high water solubilities, low Henry's law constants, and low KO, values. Herbicides with a KO, less than about lo4 do not partition to organic rich soils to any great extent (6,10, 12, 27). These compounds move from the outer root to the inner root, are drawnintotheplant bythexylemwithshortresponse times, and are distributed within the plant depending on their lipophilicity (s). As hydrophilic compounds are translocated within the plant, they can be significantly metabolized (10,241. For example, using 14C-labeled parent compounds under controlled exposure conditions, Trapp and co-workers found that the metabolism of atrazine was as high as 60% in barley plants (Hordeum vulgure) (24). Of the metabolites found in plants, approximately 82%were polar metabolites and 18% were insoluble in methanol (24). Although not directly measured, these authors speculated that the degradation products were hydroxylated derivatives and dealkylated products of atrazine. In addition, these authors observed a greater fraction of metabolites in plants than in soil, which may be due to enzymatic reactions within the plant. However, only 0.5% of the 14Cwas converted to COz by the plants (24). Lipophilic Compounds. Most lipophilic organic pollutants (KO, greater than approximately lo4) [such as polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/F),organochlorine pesticides, polychlorinated biphenyls (PCBs), and polycyclic aromatic hydrocarbons (PAHs)]partition to the epidermis of the root or to the soil particles and are not drawn into the inner root or xylem (6, 19, 27, 28, 31, 42).
There are a few exceptions however. Arecent field study by Hulster and co-workers has shown that zucchini (Cucurbita pepo L. convar. giromontiinu cv. Diamant F1) and pumpkins (Cucurbita pepo L. cv. Gelber Zentner) 2906
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accumulate and translocate higher concentrations of PCDD/Fs from contaminated soil than other fruits and vegetables, and this is the main contamination pathway for these species (36). Zucchini, pumpkin, and cucumber plants were grown next to one another, under field conditions, in various combinations of uncontaminated and PCDDIF-contaminated soil. These authors were able to compare plant PCDD/F concentrations and profiles to the contaminated soil, uncontaminated soil, and air PCDD/F concentrations and profiles (36). Although the primary route of uptake for cucumber plants was from the atmosphere, zucchini and pumpkin plants clearly showed uptake from PCDDIF-contaminatedsoil. This may be due to root exudates, unique to these species, that mobilize PCDD/F from the soil particles and make these compounds available for uptake (36). For most species examined, however, many controlled exposure experiments and field experiments have shown that the uptake of lipophilic organic pollutants through roots is not a significant pathway of accumulation (19,24, 27,28, 31, 35, 40, 4 1 ) . In general, lipophilic pollutants are not translocated within the plant, and metabolism is not significant (24). Air to Plant. The main accumulation pathway for lipophilic organic pollutants is from the air to the leaf surface. As shown in Figure 1, the degree to which these pollutants accumulate in the leaf is dependent on vaporparticle partitioning in the atmosphere, the octanol-air partition coefficient (Koa),and the plant species (7,20,22, 26,37,43). The lipid concentration and surface area of the leaf also influence the degree of accumulation (22,26,37). The partitioning of lipophilic pollutants from the outer leaf to the inner leaf is slow (this will be discussed later), and rarely are these compounds transported by the phloem. In general, gas-phase pollutants with a large Koaare preferentially accumulated ( 7 2 0 , 37). Gas or ParticleDeposition. Although controlled exposure experiments work well for studying plant uptake from soil, field experiments are required to fully address atmospheric gas-phase or particle-phase deposition to leaves. A combination of field and near-field experiments was recently published by Welsch-Pausch and co-workers, which represents an effort to minimize variables under field conditions (35). As shown in Figure 2, a series of simultaneous outdoor and greenhouse plots of Welsh ray grass (Lolium multijlorum) was examined throughout the growing season in order to study dry particle-bound and dry gaseous deposition of PCDD/F. Uptake from contaminated soil was also investigated and was found to be negligible (35). The greenhouses were designed to draw in outdoor air in various combinations; gas-phase and particle-phase (greenhouse 11, gas-phase only (greenhouse 21, and clean air (greenhouse3) (35). This allowed for direct comparison to grass grown in the outdoor plots (plots 1-3). However, there were substantial chamber effects: loss of large particles ('3 pm) in the air ducts was observed in greenhouse 1; elevated temperatures in the summer resulted in abnormally high gas-phase air concentrations in greenhouse 2 from desorption of compounds on the particle removal filter; and the activated carbon used to clean the outdoor air in greenhouse 3 was not effective. Although data from greenhouse 3 had to be discarded, the authors were able to salvage some data from greenhouses 1and 2 that had been collected in the summer and autumn (35).These authors found that dry gaseous deposition was
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FIGURE 2. Experimental approach used by Welsch-Pausch and co-workers. Taken from ref 35.
the principal pathway of Cb-C16PCDD/F accumulationin the grass leaves. Although deposition of large panicles was an important pathway for uptake of Ch and Cla PCDD in the autumn, dry deposition of small particles (c3pm) was found to be negligible ( 3 3 . Other attempts to understand atmospheric deposition under field conditionswere recentlypublishedhy Simonich and Hites (37)and Nakajima and co-workers (39). In both cases, deposition of polycyclic aromatic hydrocarbons (PAH) to plant surfaces [needles, leaves, seeds, and bark from sugar maple (Acer saccarum) and white pine (Pinus strobus) trees (37) and azalea leaves (Rhododendron oomurasakn (39)l was studied under natural conditions, throughout the growing season. Simultaneous PAH concentration measurements in air allowed for direct comparison to the PAH concentrations and profdes measured in the vegetation. Data interpretation for these experiments requires rigorous statistics because there are many variables that can influence the uptake by vegetation. Both groups of researchers modeled atmosphere-vegetation partitioning of PAH using a form of the Yamasaki equation (44, 43, assuming that vegetation acts as a particle. Simonich and Hites calculated a vegetation-atmosphere partition coefficient for the individual PAH using
where veg is the concentration of PAH in vegetation (ng/g dry wt); lipid is the lipid content of the vegetation, which is a measure of the total capacity for sorption of PAH to vegetation (mg/g drywt); gas is the atmospheric gas-phase PAH concentration prior to collection of vegetation (ng/ m3); a is the common y-intercept; and Tis the ambient temperature (K) (37). Multiplying the slope, al, by the gas ConstantgivesthePAH-vegetationhindingenergy,Q d (37). Nakajima and co-workersapplied the inverse of eq 1, with the lipid correction term omitted (39). Both groups showed that the partitioning between the atmosphere and vegetation is dependent on ambient
temperature [averagedover 5 days prior to collection (37) or 1 month prior to collection (3911 and the gas-phase atmospheric PAH concentration. At low ambient temperatures (autumn and winter), PAH partition to vegetation, and at high ambient temperatures (summer), some PAH volatilize back to the atmosphere. Although panicle-phase PAH are found in vegetation, the predominate pathway is gas-phase deposition (37, 39). Although the Welsch-Pausch et al. study experienced chamber effects (35) and the Simonich and Hites (37) and Nakajima etal. (39)experiments required rigorous statistics for interpretation, these studies successfully investigated atmospheric deposition to plant surfaces under field conditions. Untilaselective extractionmethodis developed that removes onlyparticle-bound pollutants from the plant surface, additional indirect studies, such as these, are required to investigate panicle-phase versus gas-phase deposition to plant surfaces. Octanol-Air Partition Coefficient. The octanol-air partition coefficient (Koa)has become a key parameter in the understanding of pollutant sorption to leaf surfaces. Koa can be calculated from the compounds air-water panition coefficient (Henry’s law constant) and KO, (7) or measured directly (46). Given that KO, is a measure of a compounds preference for octanol (or the plant wax) over the air, &a should he strongly related, under equilibrium conditions, to the ratio of the concentration of lipophilic pollutant measured in the plant to the concentration measured in the air; this is the so-called bioconcentration factor (BCF,,,). The use of BCF,,, implies that equilibrium has been achieved; however, this is frequently only an optimistic assumption. Figure 3 shows the relationship between the logarithm of the unitless BCFDI,and the logarithm of the corresponding KO, for three different studies. The data in Figure 3 were taken from a compilation of controlled exposure experiments using greenhouses by Paterson et al. (7). controlled exposure experiments using a fugacity meter by Tolls and McLachlan (201, and a field study conducted over the growingseasonby SimonichandHites (37). TheBCF,), and &a values for the Paterson et al. and Tolls and VOL. 29, NO. 12.1995 I ENVIRONMENTAL SCIENCE & TECHNOLOGV
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FIGURE 3. logarithm of the bioconcentration factor between plant and air (BUM,) versus the logarithm of the octanol-air partition coefficient (Koa).KO,values for Simonich and Hites data (37) were calculated from the Henry's law constants and octanol-water partition coefficients at 25 "C (47).The correlation coefficients are given; all are significant ( P< 0.01).
McLachlan data were taken directly from the publications, while the BCFpiavalues for the Simonich and Hites data were determined by multiplying the K, values calculated in eq 1 (at 25 "C) by the air density. The Koa values for the Simonich and Hites data were calculated by multiplying the KO, value (47) by RT and dividing by the corresponding Henry's law constant (at 25 "C). The BCFplaand corresponding Koavaluesgiven in Figure 3 represent awide range of compounds [chlorinated organics (7,201,herbicides (7), and PAH (20,37)] and plant species [azalea (7), Welsh ray grass (20), and needles, leaves, and tree bark (331. As shown in Figure 3, both the controlled exposure studies (7, 20) and the field condition study (37) indicate that Koa is a good predictor of lipophilic pollutant accumulation in leaves. Clearly, the BCFp/a is strongly correlated with Koain all of these studies, indicating that the relationship is valid for a wide range of lipophilicorganic compounds, plant species, and field conditions. However, the greenhouse studies (7,ZO)may overpredictleaf pollutant concentrations versus field conditions (37). The slope of the regression for the Paterson et al. and Tolls and McLachlan data are 0.907 and 0.999, respectively, while the slope of the Simonich and Hites data is 0.481. This difference may be due to additional variables, such as fluctuations in ambient temperature and air pollutant concentrations, that effect pollutant accumulation under field conditions but that may not be present under controlled exposure conditions. Different types of vegetation were also used in these studies. This discrepancy confirms the need to validate empirical models and controlled exposure experiments under field conditions. Clearly, additional studies are needed to investigate the relationship between BCFplaand Koa. Given the importance of KO,in determining the partitioning of lipophilic pollutants from the air to the plant surface, it is important to have an accurate measure of this partition coefficient. Although Koa has been routinely calculated from Henry's law constants and KO, values in the past, it is difficult to estimate its temperature dependence, and it is likely that this calculation is not accurate given the propagation of experimental error. Recently, Harner and Mackay developed a method for the direct measurement of Koavalues(46). These measurements were 2908
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FIGURE4. Total PAH concentration over the growing season on (a) gram dry weight vegetation basis and (b) lipid-adjusted basis.Taken from ref 37.
made by passing air saturated with octanol through a glass wool column coated with a solution of the compound in octanol and then measuring the compound in the outlet air by collecting it on an absorbent trap. These authors were able to measure Koavalues for chlorinated benzenes, PCBs, and DDT between -10 and +20 "C (46). In general, there was reasonable agreement between the calculated and measured Koavalues, although the ratio increased for the more lipophilic compounds (such as PCBs). Harner and Mackay suggest that Koabe measured directly rather than calculated, especially for highly lipophilic organic compounds (46). In addition, Harner and Mackay have shown that Koais strongly dependent on temperature (46). Their results indicate that Koaincreases by a factor of about 30 from - 10 to +20 "C (46). This is significant because it indicates that the change in Koawith temperature must be considered when investigating sorption to leafsurfaces. It is particularly important to determine the temperature dependence of Koa,and further studies are needed to measure Koadirectly for other compounds. In addition, BCF,,, values should be correlated against Koavalues that were measured at the same temperature as the vegetation. Lipid Concentration and Surface Area. The degree of sorption of an organic pollutant to various leaf surfaces exposed to the same air concentrations can vary greatly (26,37,38). This has been observed under both controlled exposure conditions and field conditions. Differences in accumulation can be explained, in part, by the differences in plant lipid concentration and the plant surface area available for accumulation (22,26, 37). Under field conditions, Simonich and Hites have shown that the differences in the concentration of PAH in needles, leaves, seeds, and tree bark collected from the same site can be minimized by normalizing the pollutant concentration in the plant to the lipid concentration of the vegetation (37). Figure 4a shows the average difference in total PAH concentrations in plant tissues exposed to the same air concentrations is about a factor of 5 on a dry weight basis, while it is less than 2 on a lipid basis (see Figure 4b) (37). Normalizing plant PAH concentrations to lipid content does not account for all of the biological variability, but it does
minimize it. This is especiallytrue when directly comparing different plant species and tissues. By exposing needles from different conifer species (Picea abies L. Karst., Picea pungens Engelm., Pinus sylvestris L., Abies alba Mill., and Abies koreana Wils.) to aqueous solutions of organic compounds, Schreiber and Schonherr have shown that the rates of uptake are dependent on the specific surface area of the needles (22). Needles with high surface areas showed higher rates of accumulation than did needles with lower surface areas at equal exposure concentrations (22). In addition, recent work by McCrady in which azalea (Rhododendron i n d i u m , var. Pearl Bradford), Norway spruce (Piceu abies), narrowstem kale (Brassica olerucea,var. acephala), and jalapeno pepper (Capsicum annuum) foliage were exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) showed that the uptake rate constants for the different species were related to the exposed surface area (26‘). Rate constants normalized to the plant dry weight varied by a factor of 50, while the rate constants normalized to the plant surface area varied by only a factor of 4 (26‘). The cuticular wax content of the plant did not appear to effect the short-term sorption kinetics of 2,3,7,8-TCDD(26). Given these findings, vegetation pollutant concentrations and rate constants should be normalized to the lipid concentration of the vegetation or its surface area, especially when directly comparing different species and tissues. In general, if the partitioning approaches equilibrium, the lipid content should be used, and if the partitioning is not at equilibrium, the surface area should be used since this influences the uptake rate constant. Kinetics. The kinetics of pollutant uptake in leaves has primarily been investigated under controlled exposure conditions. In these experiments, uptake is monitored by placing uncontaminated plants in a chamber containing elevated air concentrations of gas-phase pollutants. M e r hundreds of hours of exposure, the plant is placed in a clean atmosphere and clearance is monitored. Plant and air samples are collected at timed intervals throughout the uptake and clearance experiments. Previously, the kinetics ofuptake and clearancehad been described using a one-compartment model for the entire leaf without distinguishing between the outer and inner leaf (21,23,29,30). This model has become known as the “azalea model” because it has been used extensively to describe uptake and clearance of azaleas in greenhouse experiments (23, 29, 30). Although this simple model describes the long-term kinetics of the leaf, it neglects instantaneous changes in leaf pollutant concentrations that are often observed at the beginning of clearance experiments (18). Recent experiments indicate that (for some species) the kinetics of leaf or needle uptake is best explained by a twocompartment model that describes partitioning to the outer surface of the leaf and partitioning into the inner leaf separately (18,20, 22, 48). The two-compartment model includes a responsive surface compartment (the outer leaf) and a sluggish interior reservoir (the inner leaf). Initially, the majority of the pollutant is contained in the outer surface of the leaf, and then it gradually partitions into the inner compartment. Diffusion into the inner compartment is the rate-limiting step for whole leaf contamination; many authors have noted that equilibrium may never be achieved during the length of the experiments (7,18,20,21,25,43).
---ng/g dry needle
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FlGURE5. Uptake and clearance response of spruce needles exposed to p,p’-DDE contamination under controlled conditions. Taken from ref 18.
This barrier between the inner and outer compartments is illustrated in Figure 1. Recently, Hauk and co-workers demonstrated the validity of the two-compartment model (18). By exposing P. omorika and P. abies needles in chambers to gas-phase p,p’-DDE and collectingneedle and air samples throughout the uptake and clearance experiments, they were able to identify the instantaneous decrease in needle DDE concentrations at the beginning of the clearance phase (18). Figure 5 clearly shows this fast decrease in plant DDE concentration at approximately310h, followed by a gradual decrease in concentrationwith time (18). The fast response of the pine needles to changes in atmospheric contamination level is governedby sorption or desorption (depending on uptake or clearance) at the surface of the needle, which takes place on the order of hours (18, 20). The gradual increase or decrease is due to slow diffusion into or out of the inner needle compartment (14,181, which takes place on the order of hundreds of hours. Figure 5 clearly shows that the two-compartment model fits the observed kinetics much better than the one-compartment model. There have been attempts to chemically separate these two compartments from needles using selective solvent extraction methods (18, 25, 48, 49). These extractions usually involve a series of solvents of increasing polarity or a series of timed extractions. These crude procedures are difficult to reproduce, and there is no confirmation that these extraction procedures give an accurate measure of the load in the compartments. Although these procedures have been used to show that lower molecular weight organic pollutants partition into the inner compartment more readily than higher molecular weight organic pollutants (25,491,Hauk etal. concluded that these procedures were not selective enough to be applied to the two-compartment model (18). Selective solvent extractions are of limited use until more reproducible methods are developed. The fast (days to weeks) and slow (months to years) response of vegetation to changing environmental conditions, consistent with the two-compartment model, have been observed under field conditions. Under field conditions, Simonich and Hites found that new vegetation accumulated PAH quickly, within 2 weeks of emergence (37). As mentioned previously, fluctuations in the vegetation-atmosphere partition coefficient were correlated with the average ambient temperature over 5 days prior to sample collection (37). Nakajima and co-workers found that a VOL. 29, NO. 12, 1995 / ENVIRONMENTAL SCIENCE & TECHNOLOGY rn 2909
similar partition coefficientwas correlated with the average monthly temperature (39). Presumably, these relatively fast responses to temperature and initial exposure are due to accumulation by the outer leaf or needle compartment (the fast compartment). It appears to take a long time for the entire needle to reach equilibrium. Keymeulen and co-workers exposed virgin pine trees (Pseudotsuga rnenziesiz) to toluene, ethylbenzene, and xylenes under field conditions for several years (38). In most cases, it took 5-6 months for the trees to achieve equilibrium (38). This gradual development of equilibrium is presumably due to the slow partitioning of pollutants into the inner leaf. From both controlled exposure and field experiments, we conclude that vegetation is a good integrator of atmospheric pollutants. Some species have both a fast compartment and a slow compartment. Because of the large fluctuations in ambient air levels and the resistance to contamination of the slow compartment, it is unclear if equilibrium is ever achieved, especially under field conditions. Under these conditions, it appears that the outer compartment responds to fluctuations in temperature and possibly gas-phase concentrations on the order of days to weeks, while the inner compartment responds on the order of months to years. Degradation. Given that some organic pollutants are known to degrade in the atmosphere, it is important to investigate possible degradation at the plant surface. McCrady and Maggard have shown that photodegradation can be a significantremoval mechanism at the plant surface (21). These authors exposed reed canary-grass (Phalaris arundinacea L.) to gas-phase f3H1TCDDand various levels of UV radiation under controlled conditions. The photodegradation half-life of 2,3,7,8-TCDDsorbed to grass and exposed to natural sunlight was 44 h, while the half-life resulting from volatilization of the pollutant was 128 h (21). These authors conclude that elimination of 2,3,7,8-TCDD by photodegradation should be considered when estimating uptake of this pollutant (21). Standley and Sweeney observed oxidation of endosulfan I and I1 to endosulfan sulfate in leaves and bark under field conditions (50). Simonich and Hites also found oxidation of endosulfan at the plant surface. They measured a ratio of endosulfan Ilendosulfan IUendosulfan sulfate concentrations in tree bark from the United States of approximately 1:0.8:3.5, but the typical ratio of endosulfans in the atmospheric gas-phase was 1:0.08:0 (51). This difference suggests that endosulfans I and I1 are isomerized and that both are oxidized to endosulfan sulfate at the plant surface. Clearly, degradation at the plant surface should be considered when studying pollutants that are known to degrade under environmental conditions. In addition, possible degradation should be included in models when predicting plant uptake. Care should be taken when interpreting vegetation concentration ratios to determine "recent" emission of pollutants (like the ratio of DDT to DDE), because degradation may be enhanced on the surface of vegetation.
Vegetation as Indicator of Contamination Many researchers have used pollutant concentrations in vegetation to qualitatively indicate atmospheric contamination levels. Most of these attempts have been successful because vegetation integrates contamination over time, and 2910 1 ENVIRONMENTAL SCIENCE &TECHNOLOGY / VOL. 29, NO. 12, 1995
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FIGURE 6. logarithm of trichloroacetic acid (TCA) concentrations in pine needles as a function of distance from pulp mills. The correlation coefficient is given; it is significant ( P < 0.01). Replotted from ref 53.
vegetation samples are much easier to collect than air samples, especially in remote locations. The use of vegetation to qualitatively indicate organic pollutant atmospheric contamination is valid as long as the mechanism of plant uptake is considered. As mentioned above, uptake will be influenced by ambient temperature, airpollutant concentration, plant species and lipid content, time of exposure, whether the pollutant is lipophilic or hydrophilic,and whether the pollutant is in the atmospheric gas or particle phase. In addition, there can be considerable variability within samples from the same site (20-6076 relative standard deviations are common); thus, it is advisable to collect and analyze many samples (49,52,53). Vegetationhas been used to identlfy point sources of organic pollutants (52-561, to determine regional contamination within cities, countries, and continents (43,49,50,57-691, and to determine the global contamination of organic pollutants (70- 72). Point Sources. Vegetation is particularly useful for identifying unknown point sources of pollutants as shown recently by Juuit et al. for hydrophilic trichloroacetic acid (TCA) (53). Although TCA was used until the 1960s as a herbicide, its continued presence in the atmosphere suggests yet unidentified sources (53). These authors used Scots pine needles (Pinus sylvestris L.) to trace emissions of TCA to two closely situated kraft paper mills in Finland, which used C102 as a bleaching agent (53). Samples were collected from 5 to 120 km downwind from the mills. The TCA concentrations in needles were negatively correlated with the distance from the mills; see Figure 6. These data indicate that the TCA concentrations in needles dropped dramaticallywithin 10 km of the mills, but remained above background levels for 60-80 km downwind from the mills (53). Juuti and co-workers hypothesized that the TCA was produced by reactions of volatilized Ce-chlorocarbons formed during pulp bleaching (53).Another possibility is that TCA may have volatilized directly from spent bleach liquors during the sewage treatment process (53). Using spruce needles to indicate pollutant contamination levels, these authors have shown that kraft pulp mills are sources of TCAwhen chlorine-containingbleaching agents are used. Meredith and Hites (54) and Hermanson and Hites (52) used blackwalnut (luglausnigra),tulip poplar (Liriodendron tulipifera), white oak (Quercus alba), sugar maple (Acer saccarurn), and red maple (Acer rubrurn) tree bark to investigate polychlorinated biphenyl (PCB)concentrations
near S u p e h d sites in Indiana. Meredith and Hites initially planned to use the annual growth rings of the tree trunk to determine historical PCB contamination,but they found that all of the PCBs were contained in the outer 1 cm of bark (54). Both Meredith and Hites (54) and Hermanson and Hites (52) found that the PCB concentrations in tree bark decreased dramatically with distance from the Superfund sites. Concentrations dropped by a factor of about 10withinllkm (52)andbyafactorof40within14km(54). Both studies show that tree bark can be used to indicate pollutant contamination levels. Safe and co-workers have also shown that vegetation can be used to identlfy pollutant sources by analyzing pine needles for PCDD/F near two pentachlorophenol woodpreserving sites in Montana and Texas (55). Samples were also collected from remote areas for comparison. As with the previously mentioned studies, Safe et al. found a rapid decrease in total PCDD/F levels in pine needles with increasing distance from the source (55). The level of octachlorodibenzo-p-dioxin dropped by a factor of 6 within 1km of the site’s perimeter (55). In addition, the PCDD/F distribution profile in needles collected at the woodpreserving sites resembled the profile in commercially available pentachlorophenol, while the needles collected from remote sites resembled the PCDD/F profile in the atmosphere (55). All of these studies indicate that vegetation can be used to pinpoint local pollutant sources. Regional Contamination, Vegetation has also been used to indicate ubiquitous pollutant contamination levels. In order to determine the general contamination level of cities, countries, and continents, many samples from a variety of locations are required in order to minimize the effect of point sources and overcome the inherent variability of samples from the same site. A series of papers by Kylin and co-workers has outlined the use of Scots pine (P.sylvestris L.) needles to determine the regional contamination of organochlorines in Europe (49, 57, 67, 68). Jensen et al. collected pine needles from France, Switzerland, Germany, Denmark, Poland, Czechoslovakia, Sweden, and Norway in 1986 and analyzed them for DDT, hexachlorocyclohexanes (HCHs), pentachlorophenol (PCP),PCBs, and hexachlorobenzene (HCB) (68). They tracked DDT concentrations in needles to the use of DDT in the former East Germany, while most HCHs, PCBs, and HCB were ubiquitous throughout Europe (68). However, the concentrations of PCP were elevated in needles from Sweden, and lindane (y-HCH)was elevated in samples from southern France (68). These researchers collected needles again in 1989 from some of the same sites and analyzed them for the same compounds (excludingPCBs) (49). The results were similar to the previous study. Lindane concentrations in needles decreased slightly from south to north, while the concentrations of a-HCH and HCB were uniform throughout the sites (49). The ratio of DDT to DDE decreased from south to north, and the concentration of PCP in north Sweden samples remained high (49). This study also showed that sampling at a consistent height within the tree is preferred, that there is no difference in needle pollutant concentration of trees facing different directions, and that the age of the tree does not influence the needle pollutant concentration (49). Calamari et al. used pine needles to determine regional contamination of DDTs, HCHs, and HCB in Europe (58). Samples were collected from Italy, Holland, Austria,
Finland
30
Czechoslovakia
Greece
I
C
FIGURE7. Organochlorine insecticide concentration in pine needles from Finland, Czechoslovakia, Italy, and Greece. Replotted from ref 58.
Czechoslovakia, Finland, and Greece. The measured needle organochlorine concentrations were compared to previous studies in other European countries. These authors suggested that the organochlorine distribution pattern, or “fingerprint”, in pine needles from a given country is dependent on use of the compounds in that country and on its socioeconomic conditions (58). Figure 7 shows the organochlorine insecticide concentrations in needles from some of the countries investigated by Calamari and co-workers (58). There is a wide range in organochlorine concentrations among the countries. As shown in Figure 7, Czechoslovakia was the most contaminated country of those sampled, while Finland was the least contaminated (58). The Czechoslovakia and Greece fingerprints are not characterized by any particular insecticide, while the Finland fingerprint is characterized by a-HCH and the Italy fingerprint is characterized by p,p’DDT. Calamari and co-workers conclude that the “fingerprint” gives information on the technology level of the agriculture, the effectiveness of insecticides bans, the age of contamination, and the role of long-range transport (58). Other such studies have used vegetation to determine regional contaminationinAfrica (61,631,Canada (661,Costa Rica (501, and the Antarctic (60). Although most of these studies analyzed a relatively small number of vegetation samples collected from a limited number of sampling sites, they do show that vegetation can be used as an indicator of regional contamination levels. Jones and co-workers have shown that vegetation can also be used to indicate historical contamination levels (59, 64,65). By analyzing archived herbage samples collected between 1861 and 1989 from Rothamsted Experimental Station in the United Kingdom, they were able to determine the deposition of PAH, PCBs, and PCDD/F to vegetation over time (59, 64, 65). These studies indicate that the concentrations of PAH, PCBs, and PCDDlF in herbage samples have decreased in recent years (59, 64, 65). For example, the highest herbage PAH concentrations were measured between 1930 and 1955, but the concentrations have decreased slightly since then (64). Concentrations of lower chlorinated PCBs decreased by a factor of 50 between 1965-1969 and 1985-1989, while the higher molecular VOL. 29, NO. 12. 1995 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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weight PCBs showed a slight decrease over this same time period (65). PCDD/F concentrations in herbage also show a slight decrease in recent years, which is consistent with sediment records (59). These studies show that vegetation is useful in determining regional contamination and, if collected over time, can indicate contamination histories. Global Contamination. A few studies have expanded the use of vegetation to indicate contamination on a global scale (70-72). In order to draw conclusions on a global scale, it is particularly important to collect many samples from awide range of countries, latitudes, and climate zones. Researchers have used plant leaves and lichens (71, 72) and tree bark (70) from throughout the world to determine the global distribution of organochlorines. Calamari et ul. compared the concentrations of HCB, DDTs, and HCHs in mango leaves (Mungiferu indica), lichen, and moss samples collected from 26 sampling sites distributed globally (72). The latitude of these sites ranged from 78" N to 74" S (72). Global plant concentrations of DDTs and HCHs were relatively high (0.5-100 ng/g dry weight), while the plant concentrations of HCB were relatively low (0-1 ng/g dry weight) (72). Although these authors did not account for plant lipid concentration or surface area, they found evidence of global distillation for the relatively volatile HCB (72). Vegetation from arctic regions contained much higher HCB concentrations than vegetation from equatorial regions (72). This can be explained by the global distillation effect: HCB volatilizes from warm, equatorial regions; is transported by the atmosphere; and condenses out at colder, high latitudes. These researchers did not observe global distillation of the other organochlorine compounds measured in the study. For example, plant DDT concentrations were highest in tropical and subtropical areas, while plant HCH concentrations in the Northern Hemisphere were higher than the Southern Hemisphere (72). Simonich and Hites investigated the global distribution of 22 potentially harmful organochlorine compounds in more than 200 tree bark samples from 90 sites worldwide (51,70). They found that concentrations of relativelyvolatile organochlorine compounds, such as HCB, a-HCH, y-HCH, and (to a lesser extent) pentachloroanisole were significantly correlated with latitude. These concentrations were lower in equatorial regions compared with those in boreal and arctic regions, showing evidence of global distillation. Less volatile organochlorine compounds, such as endosulfan, were not as effectively distilled and appeared to remain near the original region of use. The distribution of the less volatile compounds is more likely related to the socioeconomic conditions of a given country (51,58, 63) or to the types of crops grown there (51). From these studies, it is clear that vegetation can be used to identlfypoint sources and to qualitativelydetermine regional and global contamination levels of organic pollutants. This is valid as long as the mechanism of plant uptake of organic pollutants is considered. Researchers must keep in mind the effect oftemperature, vapor-particle partitioning, air concentration, plant species, and lipophilicity on the uptake of organic pollutants by plants. We recommend that plant pollutant concentrations be normalized to the plant lipid concentration or surface area, especiallywhen comparing concentrations in differentplant species. This is particularlyimportant in regional and global studies when a single species of plant may not be available at all sampling sites. Finally, many vegetation samples 2912 m ENVIRONMENTAL SCIENCE &TECHNOLOGY 1 VOL. 29, NO. 12. 1995
1
Sources
j
3.94
lAtmosphere1 0.2
0.2
1
jSedimentl1
Soil
I Transport & Transformation
FIGURE 8. Total PAH flow rates (in units of 106 kg/yr) for the northeastern United States. Taken from ref 73.
should be collected and analyzed from a wide distribution of sites for regional and global contamination studies. This will help to minimize the effect of point sources and overcome the variability of samples from the same site.
Vegetation as a Pollutant Sink Given the surface area and associated lipids of plants, many researchers have speculated that vegetation may be a significant sink for lipophilic organic pollutants (1,4,6,20, 37, 43, 72, 73). By rough calculation, Morosini et al. predicted that 7 x IO8km2ofvegetation surface is in contact with the atmosphere globally (43). These authors estimated that for a typical beech forest, the ratio of the concentration of semivolatile organic pollutants in 10 m3 of leaves to the concentration in 10 m3 of air is approximately 80 for HCB and the HCHs and approximately 1600 for DDTs and PCBs (43). Several studies have shown that forests are effective air filters of organic pollutants (74, 75). Smith and co-workers measured the concentration of PCBs and DDTs in forest soils from remote northern New England hardwood and montane forests (74). These authors estimated a total PCB loading of 2.6 kg/ha and a total DDT loading of 0.9 kg/ha to forest soil (74). By studying forests in Germany, Matzner and co-workers estimated that between40 and 70%of total PAH deposition to forest floors comes from leaf litter (75). Under spruce forests, litter fall accounts for 40-70% of the total PAH deposition, while 30-50% is accounted for under beech forests (75). Clearly,vegetation removes a substantial amount of lipophilic organic pollutants from the atmosphere. It is likely that vegetation is an essential part of the annual cycling of these compounds and may act to decrease their atmospheric residence times (37, 73). Although the role of vegetation as a pollutant sink is an important issue, only one study has attempted to quantitatively estimate the magnitude of vegetation as a sink for lipophilic organic pollutants. A preliminary mass balance of PAH in the northeastern United States has been developed by Simonich and Hites for this purpose (73). The area of this region is approximately 3.3 x 106 km'. Approximately 10% of this area is the Great Lakes; about 70% is covered by crops, grasslands, and urban vegetation; and 20% is forested (73). In addition, approximately 52% of the U S . population lives in this region (73). The mass balance shown in Figure 8 was developed based on measurements of PAH in soil andvegetation from one site within the mass balance region and on published values for PAH concentrations and fluxes in air, water, sediment, and soils (73). The authors assumed an average vegetation surface area (or "leaf area index") of 7 mz of vegetation/m2 of land and steady-state conditions. An
average total PAH areal concentration of 5.1 ng/cm2 for crops, forests, and urban vegetation and 20.1 ng/cm2 for forests was also assumed. Approximately 3.9 x IO6 kg/yr of PAH is emitted by sources within the mass balance region and is removed from the atmosphere by wet and dry deposition to bodies of water, vegetation, and soil, while the remainder is transported out of the mass balance region or transformed (73). This model estimates that 44 & 18% of the PAH emitted into the atmosphere from sources in this region is removed by way of vegetation annually (73). Clearly, this is a rough estimate which warrants further study. This mass balance model estimates the average removal of PAH by way of vegetation for an area of the world with 10% water and 90% land and vegetation. The removal rate will change depending on the time of the year (ambient temperature) and the surface area of vegetation (the percent of land area covered with vegetation and the leaf-area index). However, even given the errors associated with this preliminary model, the results indicate that vegetation is a major sink for lipophilic organic pollutants.
Recommendations Vegetation is the link between the atmosphere and the human food supply. Thus, it is important to understand those processes by which pollutants enter this environmental compartment. Although early research was intermittent and exploratory, significant advances have been made in the last 5-7 years. Because of the complexity of the plant matrix, the use of modern extraction, purification, and analysis methods has been necessary to advance this field. While the mechanism of plant accumulation is understood to some extent, we recommend more field studies involving native plants. Empirical and controlled exposure models should be validated under field conditions. As discussed earlier, several controlled exposure models may overpredictuptake under field conditions. In addition to different plant species, there are many variables present under field conditions that cannot be readily duplicated in controlled exposure experiments. As Nellessen and Fletcher note, a disproportionate amount of work has gone into studying the uptake of pesticides by crop species; more studies need to be done on the uptake of industrial pollutants by native plants ( 1 ) . Vegetation can be successfully used as a qualitative indicator of organic pollutant atmospheric contamination as long as the mechanism of accumulation is considered. Researchersmust understand the influence of lipophilicity, ambient temperature, plant species and lipid content, and vapor-particle partitioning on plant pollutant concentrations. We recommend that plant pollutant concentrations be normalized to the plant lipid concentration or surface area, especially when directly comparing different species. Finally, very little is known about the magnitude of vegetation as a sink and its effect on the atmospheric residence times of lipophilic organic pollutants. The role of vegetation as a sink will be influenced by its area, time of the year, lipophilicity of the organic pollutant, and whether the pollutant is present in the atmospheric gas or particle phase. Additional studies are required to investigate this issue.
Acknowledgments We thank Michael Simonich for assistance with the plant biology.
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Received for review June 5,1995. Revised manuscript received September 12, 1995. Accepted September 12, 1995.@ ES950382M @Abstractpublished in Advance ACS Abstracts, October 15, 1995.
