Environ. Sci. Technol. 2005, 39, 2494-2499
Organochlorine Pesticides in Agricultural Soil and Vegetables from Tianjin, China S . T A O , * ,† F . L . X U , † X . J . W A N G , † W. X. LIU,† Z. M. GONG,† J. Y. FANG,† L. Z. ZHU,‡ AND Y. M. LUO§ Laboratory for Earth Surface Processes, College of Environmental Sciences, Peking University, Beijing 100871, China, Department of Environmental Science, Zhejiang University, Hangzhou 310028, China, and Institute of Soil Science, CAS Nanjing, Jiangsu 210008, China
Samples of eight types of vegetables, the rhizosphere soils, and bulk soils were collected from two sites (A and B) in Tianjin, China for the determination of hexachlorocyclohexane isomers (HCHs) and dichlorodiphenyltrichloroethane and metabolites (DDXs). The average concentrations of total HCHs and DDXs in the bulk soils were 3.6 and 80.1 ng/g for site A and 102 and 235 ng/g for site B, respectively. Relative accumulations of HCHs and DDXs in the rhizosphere soil from site A but not site B were demonstrated. The concentrations of total HCHs and DDXs in vegetable roots were 3.6-60 and 4.2-73 ng/g for site A and 15-152 and 7.1-136 ng/g for site B, respectively. Difference in bioaccumulation among various vegetables, especially between tuber and fibrous vegetables was significant. DDXs in spinach and cauliflower from site B and lindane (γHCH) in cauliflower from both sites and violet from site B exceeded the maximum residual limits. Linear correlation of log-transformed HCHs and DDXs contents between the vegetable roots and the rhizosphere soils suggests the direct uptake of HCHs and DDXs.
Introduction Hexachlorocyclohexane isomers (HCHs) and dichlorodiphenyltrichloroethane and metabolites (DDXs) have been used extensively in China, resulting in widespread environmental occurrence (1,2). Agricultural application of HCHs and DDXs in Tianjin lasted from 1953 to 1993, with large quantities applied (1,3). In addition, wastewater discharged from several large pesticide producers added large quantities of HCHs and DDXs to local loadings (3-5). The facilities for technical HCHs and lindane production were not shut down until the end of 2000, while DDT production is still underway. The wastewater from their out-of-date production lines was not well treated. As a result, agricultural soils in the area have been severely contaminated, while various kinds of vegetables grown in the area supply the local market and neighboring provinces. Results of a recent survey indicated that levels of total HCHs and DDXs in the surface soils of the area were 45.8 ( 141ng/g and 56.0 ( 133 ng/g, respectively (6,7). Since food is a major source of human exposure to persistent organic pollutants (8) and vegetables are a basic food in the * Corresponding author phone and fax: 0086-10-62751938; email:
[email protected]. † Peking University. ‡ Zhejiang University. § Institute of Soil Science. 2494
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Chinese diet (9), scientists and local authorities are concerned with how much HCHs and DDXs can potentially accumulate in the vegetables produced in such a heavily contaminated area. Bioavailability and bioaccumulation of persistent organic pollutants depend very much on the physicochemical properties of the soil, especially at the root-soil interface, often referred to as rhizosphere soil with 1-2 mm in thickness (10-12). Difference of persistent organic pollutant concentration between rhizosphere and bulk soils has also been reported (13-15). Natural organic matter has been shown to be important in mobility of organic pollutants in soil. It was demonstrated that retention of PAHs was increased by the presence of soil organic matter (16), while the water solubilities of DDT and lindane were enhanced significantly when dissolved organic matter (DOM) was present in the soil (17). In addition, the interaction between DDXs and soil organic matter may reduce the bioavailability of the pesticides to wheat roots during uptake (18). In the Tianjin area, an important feature of the contaminated agricultural soils is the high level of organic matter resulting from the use of wastewater irrigation and occasional sludge application. The objective of this study was to investigate the levels and distribution patterns of HCHs and DDXs in various types of vegetables, their rhizosphere soils, and bulk soils from two sites in Tianjin, China. Differences in accumulation of HCHs and DDXs between the two sites, between the bulk and rhizosphere soils, and among vegetable species were addressed. The influence of soil organic matter was also examined.
Methodology Sampling. Vegetable and soil samples were collected in September, 2002 from two sites in Tianjin. Site A (39°05′25′′N, 116°56′05′′E) is approximately 3 km away from the nearest industrialized area, with no history of wastewater usage in irrigation. Site B (39°02′54′′N, 117°08′36′′E) is less than 0.5 km from the urban district of Tianjin with a 40-year history of wastewater irrigation. Histories of vegetable growth at site A and site B were 30 and 40 years, respectively. They were commercial sites operated under collective farms at the beginning and were converted into home gardens 20 years ago. A variety of vegetables are grown at both sites, usually in small pieces of field of several hundreds of square meters in size for each vegetable. As a common practice, the fields are rotated for different vegetables every year. Soils at both sites were median textured silty loam and slightly alkaline with pH values of 7.0 (site A) and 7.1 (site B), respectively. High levels of HCHs and DDXs in surface soils from the vicinity of site B have been previously documented (6,7). At each site, a plot of 50 × 50 m2 containing a variety of vegetables was chosen. At each site, composite bulk soil samples (0-20 cm) were collected from 4 locations 40-50 m apart (200 g each) and thoroughly mixed. Two bulk soil samples were collected from each site. Eight representative vegetable species including Chinese cabbage (Brassica rapa pekinensis), Chinese spinach (Amaranthus tricolor), celery (Apium graveolens dulce), sweet violet (Viola odorata), cauliflower (Brassica oleracea botrytis), turnip (Brassica rapa), carrot (Daucus carota sativus), and broad beaked mustard (Brassica rapa narinosa) were sampled. The vegetables were removed from the soil and mildly shaken to remove soil loosely adhering to the roots. The remaining adherent soil was then separated from the roots by washing using distilled water as rhizosphere soil sample. After harvest and transportation to the laboratory, the vegetable samples were 10.1021/es048885s CCC: $30.25
2005 American Chemical Society Published on Web 03/09/2005
thoroughly washed with running tap water to remove airborne dust and soil particles. The vegetables were freezedried (Eyela FDU-830) and pulverized to pass through a 40mesh sieve. The root and aerial parts of the vegetable were separated, and 5-10 stands of each vegetable as subsamples were thoroughly mixed to form a composite sample by sieving through the sieve four times. Soil samples were air-dried at room temperature and ground (Fritsch Pulveristte 2) to pass through a 70-mesh sieve. Two rhizosphere soils, two aerial parts, and two root samples were collected for each vegetable species at each site. All samples were kept frozen at -18 °C until analysis and were subject to measurement of R-HCH, β-HCH, γ-HCH, δ-HCH, p,p′-DDT, p,p′-DDE, p,p′-DDD, o,p′DDT, o,p′-DDE, and o,p′-DDD. Extraction and Cleanup. The soil samples were extracted using accelerated solvent extraction (Dionex, ASE 300). A 20-g soil sample mixed with anhydrous sodium sulfate was extracted in a 34-mL stainless steel vessel with 1:1 n-hexane/ acetone at 100 °C and 1 500 psi for a 5-min heat-up followed by a 5-min static extraction. The vessel was then rinsed with 17 mL of the same solvent. The extracts were cleaned with 15 mL of fuming sulfuric acid in a separatory funnel, and then cleaned twice with 100 mL of 4% anhydrous sodium sulfate solvent. Elemental sulfur was removed by adsorption onto activated copper powder. A chromatography column (10 mm inside diameter × 150 mm length) was filled with n-hexane. Florisil (5 g) was added, and the column was covered with a layer of quartz sand mixed with anhydrous sodium sulfate to a depth of 20 mm. The ASE extracts were concentrated to about 3 mL in a vacuum rotary evaporator at a temperature below 38 °C, and the remaining extracts were transferred to the Florisil column, followed by elution with a mixture of 100 mL of 90% n-hexane and 10% acetone at a rate of 1-2 mL/min. The eluate was concentrated to near dryness in a vacuum rotary evaporator, then diluted with n-hexane, and brought to exactly 1.0 mL by nitrogen blowdown (Eyela MG-1000) at room temperature. The samples were sealed in vials and stored at -4 °C before analysis. The vegetable samples were also subjected to accelerated solvent extraction. The procedure was similar to that for the soil samples except that 5 g of dried sample from the well mixed composite sample was used. The extract was concentrated and transferred to a 250-mL separatory funnel with 40 mL of n-hexane. A total of 40-60 mL of concentrated sulfuric acid was added several times for sulfonation. The sulfonated extract was mixed with 4% sodium sulfate solution twice prior to Florisil column chromatography and concentration in an identical procedure for soil sample extracts. Analysis and Quality Assurance. Samples were analyzed using an Agilent gas chromatograph 6890 equipped with a Nickel 63 electron capture detector (µECD) and a HP-5 column (30 m × 0.32 mm inside diameter, 0.25 µm film thickness). The samples were injected by autosampling at 50 °C in splitless mode with a venting time of 0.75 min. The oven temperature was programmed to first increase from 50 to 150 °C at 10 °C/min and then to increase at 3 °C/min to 240 °C, where the temperature was maintained for 15 min. Nitrogen was used as both carrier (1 mL/min) and makeup gas (60 mL/min). The injector and detector temperatures were 220 and 280 °C, respectively. A mixed working standard was used for calibration. Mirex was used as the internal standard which was added prior to the extraction. Recoveries of R-HCH, β-HCH, γ-HCH, δ-HCH, p,p′-DDE, p,p′-DDD, p,p′-DDT, o,p′-DDE, o,p′-DDD, and o,p′DDT by this method with fortified samples from Tianjin rural area were 72.8, 93.2, 79.1, 73.2, 79.0, 85.0, 90.8, 80.0, 80.0, and 93.1%, respectively. The detection limits for both soil and vegetable samples were 0.025 ng/g for p,p′-DDT and o,p′DDE, 0.015 ng/g for p,p′-DDD, 0.005 ng/g for p,p′-DDE, 0.0025
TABLE 1. TOM and DOM of the Rhizosphere and the Bulk Soils from the Two Sites TOM, mgC/g
DOM, mgC/ kg
site
bulk soil
rhizosphere soil
bulk soil
rhizosphere soil
A B
9.3 ( 0.04 32.9 ( 0.14
11.4 ( 0.13 40.6 ( 0.31
5.2 ( 0.40 8.4 ( 0.45
6.6 ( 2.05 10.7 ( 3.61
ng/g for R-HCH, γ-HCH, δ-HCH, and o,p′-DDD, and 0.0005 ng/ g for β-HCH and o,p′-DDT, respectively (6,7). A procedural blank was run with every set of 20 samples to check for contamination from solvents and glassware. All samples were extracted and analyzed in duplicate. TOM and DOM of the soil samples were determined using a TOC analyzer (Shimadzu 5000-A). DOM was extracted using fresh soil equivalent to 10.0 g of dry material in a 150-mL flask containing 50 mL of CO2-free distilled water for 2 h. The extracted supernatant was separated by filtration through 0.45 µm filter (15). Reagent and Glassware. The mixed sock standard was prepared by diluting a commercial standard (in methanol, Chem. Service Co.) with n-hexane. The working standard solutions were diluted in n-hexane. Solvents and reagents used included n-hexane (pesticide grade, Scharlan Chemies S.A. Spain), acetone (pesticide grade, Tedia Co. Inc., USA), sulfuric acid, granular anhydrous sodium sulfate, and quartz sands (analytical grade, Beijing Chemical Reagent Co.). All solvents were distilled-in-glass (PR grade) and checked for interference prior to use. Florisil (60-100 mesh, PR grade) was activated at 130 °C for 24 h and then kept in a sealed desiccator before use. Granular anhydrous sodium sulfate and quartz sands were heated at 650 °C in a furnace for 6 h and stored in the sealed desiccator. All glassware was cleaned in an ultrasonic cleaner (KQ-500B, Kunshan Ultrasonic Instrument) and heated at 350 °C for 12 h.
Results and Discussion TOM and DOM in the Soils. The measured TOM and DOM of both the bulk and the rhizosphere soils from the two sites are listed in Table 1. The statistics for the rhizosphere soils were derived based on the measured results of the 8 vegetables (two samples for each species), while only averages of two samples from each site were derived for the bulk soil. Long-term wastewater irrigation and sludge application at site B brought in a huge amount of organic matter, while there was no history of wastewater irrigation at site A. As a result, the levels of TOM and DOM, especially the former, in the soil samples from site B were much higher than those from site A (significant at 2% based on paired t-test). For both sites, there were also relative accumulations of TOM and DOM in the rhizosphere soils compared to the bulk soils. The significant levels of the one-sample t-tests for comparison between the rhizosphere and the bulk soils were 0.00 and 0.00 for TOM and 0.10 and 0.09 for DOM for the two sites, respectively. Plant roots and micro-organisms at rhizosplane are known to release considerable amounts of soluble organic matter into rhizosphere and are the primary reasons creating relatively high levels of DOM (19). DOM in the soil solution may also be brought toward and accumulate in the rhizosphere through water flow driven by plant absorption and transpiration activities. Levels of HCHs and DDXs in Bulk and Rhizosphere Soils. All of the target compounds were detected in the soil samples and the results are tabulated in Table 2 as arithmetic means and standard deviations. Results of a recent survey based on 188 topsoil samples indicated that average concentrations of total HCHs and DDXs in the surface soils of Tianjin were 45.8 ( 141 and 56.0 VOL. 39, NO. 8, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. HCHs and DDXs in the Rhizosphere and Bulk Soils from the Two Sites bulk soil, ng/g sample
A
B
R-HCH 0.5 ( 0.04 9.3 ( 0.04 β-HCH 2.6 ( 0.03 89 ( 1.59 γ-HCH 0.001 ( 0.00 0.04 ( 0.06 δ-HCH 0.6 ( 0.06 3.3 ( 0.02 p,p′-DDE 56 ( 1.58 148 ( 0.58 p,p′-DDD 4.4 ( 0.24 45 ( 0.15 p,p′-DDT 3.6 ( 0.22 30 ( 0.39 o,p′-DDE 12 ( 0.43 7.2 ( 0.21 o,p′-DDD 1.2 ( 0.08 2.8 ( 0.00 o,p′-DDT 2.7 ( 0.14 2.5 ( 0.03 total HCHs 3.6 ( 0.13 102 ( 1.51 total DDXs 80 ( 1.98 235 ( 0.28
rhizosphere soil, ng/g A
B
1.0 ( 0.51 4.8 ( 1.48 0.2 ( 0.37 1.1 ( 0.47 57 ( 30.4 4.6 ( 2.11 2.0 ( 1.04 15 ( 12.3 1.5 ( 1.22 2.9 ( 4.58 7.0 ( 2.24 83 ( 47.6
4.4 ( 2.07 12 ( 6.62 0.2 ( 0.33 2.9 ( 1.44 75 ( 30.9 16 ( 11.3 8.9 ( 5.57 5.6 ( 11.4 1.6 ( 1.00 2.1 ( 2.31 19 ( 7.71 109 ( 43.4
( 133 ng/g, respectively (6,7). Total DDXs at both sites and total HCHs at site B were higher than mean values in the area. According to the Quality Standard for Soil Environment issued in China, the Grade I standards for both total HCHs and DDXs were 50 ng/g, above which ecological impact may occur (20). Data listed in Table 2 suggest that total DDXs at both sites and total HCHs at site B were well exceeded the standards, even though both pesticides were banned for largescale agricultural application 10 years ago, indicating their persistence in the environment. Although wastewater was used for decades at site B, the results of a recent survey suggest that wastewater irrigation did not bring a significant amount of HCHs or DDXs into soils in Tianjin. Instead, the long history of pesticide application was the major reason for the high levels of contamination (6,7). The presence of a large quantity of TOM in the soil at site B (Table 1) is favorable for accumulation of HCHs and DDXs. The high affinity of soil organic matter for hydrophobic organic pollutants may protect the pollutants from microbial degradation and increase their persistency through sequestration (21). On the basis of the results of a multimedia fate modeling, Tao et al. suggested that inhibition of microbial degradation in soil, rather than adsorption, by the presence of organic matter is the primary factor governing the spatial distribution of phenanthrene, leading to a positive correlation between TOM and phenanthrene (22). Differences of most HCHs and DDXs compounds between the rhizosphere and the bulk soils can be seen (Table 2). The results of one-sample t-tests indicate that the differences between the rhizosphere and bulk soil concentrations were significant at the levels of 0.009, 0.000, and 0.018 for site A HCHs, site A DDXs, and site B DDXs, respectively. According to Clothier and Green, the likeliest explanation for the higher concentrations of chemicals in rhizosphere is movement of them from the surrounding soil into the rhizosphere under the influence of roots (23). Liste and Alexander determined PAH concentrations in the rhizosphere of plant and found more phenanthrene or pyrene in the rhizosphere soil than unplanted soil, suggesting that plants accumulate these compounds in the rhizosphere after facilitating their transport toward the roots (13). However, in this study, rhizosphere HCHs and DDXs were generally higher than those in the bulk soil at site A, but lower than those in the bulk soil at site B. If both the mobilization effect of DOM and the immobilization effect of the insoluble fraction of TOM are taken into consideration, the opposite difference between the rhizosphere and the bulk soil concentrations of HCHs and DDXs at site A compared to those at site B (significant levels 0.009 vs 0.381 for HCHs and 0.000 vs 0.018 for DDXs) may be explained partially by the relatively higher DOM/TOM ratio at site A (Table 1). The DOM/TOM ratio in rhizosphere soil at site A was about half of that at site B (0.58 × 10-3 vs 2496
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0.26 × 10-3), while concentration ratios of HCHs and DDXs in bulk and rhizosphere soils increased from smaller than 1 (0.51 for HCHs and 0.96 for DDXs) at site A to greater than 1 (5.4 for HCHs and 2.2 for DDXs) at site B. Although the total concentrations of HCHs at the two sites were very different, the patterns of individual compounds in the bulk soils from the two sites were similar in general with β-HCH as the dominant species, and only trace amounts of γ-HCH were detected (Table 2). HCHs were applied in the area in two formulations: technical HCHs (∼80% R-HCH and 13-15% γ-HCH) were used from 1953 to 1983, and pure lindane (99% γ-HCH) was used from 1983 to 1992. Since the removal rates of HCH isomers from soil are different, R/γ-HCH ratio can be used as an indication of the application age (24,25). Although possible fresh input of HCHs in Tianjin was suggested (7), the very high R/γ-HCH ratio (Table 2) indicates HCHs at the two sites were likely those from the historical application decades ago. There was almost no difference in the distribution patterns of DDT and metabolites between the bulk and rhizosphere soils in general (Table 2). However, the DDT/DDE ratio, which can be used as a rough estimate of the period of application (26), were significantly different (p ) 0.025) for the two sites. The DDT/DDE ratio for the bulk soil at site A (0.09) was less than half that of site B (0.21). Although degradation rates may be different from each other at the two sites due to difference in organic matter content and other factors, fresh contamination at site B cannot be totally ruled out. Industrial production of DDT and dicofol is still underway in Tianjin, and extensive usage of dicofol produced from DDT may bring DDT into local soil. Accumulation of HCHs and DDXs in Vegetables. The concentrations of total HCHs and DDXs in roots and aerial parts of various vegetables collected from the two sites are presented in Table 3 as mean ( standard deviation. The results of a two-way Anova revealed significant differences in root concentrations of total HCHs and DDXs between the two sites and among the eight vegetables at a p level of less than 0.0001. Except cabbage, total HCHs and DDXs in the vegetable roots from the heavily contaminated site B were all higher than those from the less contaminated site A. The average root concentrations of total HCHs for all vegetables were 14.4 and 55.0 ng/g dry weight for the two sites, respectively. The root-accumulated total DDXs were 23.9 and 60.5 ng/g dry weight for the two sites, respectively. Among the eight vegetables collected, three species with the lowest root concentrations of both HCHs and DDXs were mustard, carrots, and turnips, all of which are tuberous vegetables with relatively low specific root areas and low rhizosphere volume. The fibrous root system of the other five leafy or stem vegetables provided a relatively larger surface area for absorption as well as high rhizosphere volume to be affected. Actually, the average root concentrations of the total HCHs in the tuberous vegetables were 4.4 ( 0.77 and 18 ( 2.0 ng/g for sites A and B, respectively, compared to 20 ( 22.9 and 78 ( 45.7 ng/g in the fibrous root vegetables. For total DDXs, the concentrations were 5.0 ( 1.06 and 17 ( 10.0 ng/g for the tuberous vegetables and 35 ( 25.6 ng/g and 87 ( 41.3 ng/g for the fibrous root vegetables from the two sites, respectively. Although differences in HCHs and DDXs in aerial tissues of the vegetables from the two sites were observed, it is difficult to draw any conclusion on possible pathways of the pesticides entering the aerial parts. Both translocation from roots to aerial tissues (27,28) and evaporation from soil to ambient air followed by foliar uptake (29) were possible. Without solid evidences from controlled experiments, however, the relative contributions of the two pathways could not be distinguished quantitatively.
TABLE 3. Total HCHs and DDXs in Roots and Aerial Parts of Various Vegetables from the Two Sites HCHs, ng/g
DDXs, ng/g
vegetable
A root
A aerial
B root
B aerial
A root
A aerial
B root
B aerial
cabbage spinach cauliflower violet celery mustard carrot turnip
60 ( 8.48 8.9 ( 0.07 6.1 ( 0.16 19 ( 0.10 7.7 ( 0.02 4.9 ( 1.05 3.6 ( 0.43 4.9 ( 1.36
38 ( 4.44 43 ( 6.05 65 ( 1.11 35 ( 2.58 16 ( 2.12 130 ( 37.1 33 ( 1.08 36 ( 1.57
50 ( 5.34 60 ( 12.4 37 ( 0.85 90 ( 12.4 152 ( 7.74 19 ( 0.13 15 ( 1.96 18 ( 4.78
35 ( 3.74 59 ( 11.0 101 ( 10.6 80 ( 28.7 40 ( 12.3 46 ( 0.96 45 ( 4.19 48 ( 3.26
50 ( 5.05 15 ( 1.43 12 ( 0.48 73 ( 0.77 26 ( 0.04 6.2 ( 0.56 4.2 ( 0.87 4.5 ( 0.85
16 ( 1.76 16 ( 1.18 30 ( 0.06 39 ( 2.16 11 ( 1.10 30 ( 11.1 24 ( 1.33 16 ( 0.30
46 ( 3.62 58 ( 4.30 67 ( 1.50 136 ( 23.8 126 ( 7.22 7.1 ( 0.09 16 ( 5.00 27 ( 4.53
34 ( 5.75 102 ( 18.1 65 ( 9.91 47 ( 14.5 32 ( 6.77 23 ( 1.35 21 ( 0.73 55 ( 0.34
TABLE 4. Homogeneous Groups of Various Vegetables in Terms of BCF Values and Levels in the Rhizosphere Soil and Roots
Detailed maximum residual limits (MRLs) were issued by European Council for various foods including vegetables and the MRL value of total DDXs is 50 ng/g for either tuber, leafy, stem, or brassica vegetables (30). Among the edible parts of the studied vegetables (aerial parts of cabbage, spinach, cauliflower, violet, and celery and roots of mustard, carrot, and turnip), only the leaves of spinach and cauliflower from site B exceeded that limit. As to total HCHs, the MRL value was not provided for vegetables. Instead, 10 ng/g was listed as lindane for a variety of vegetables. According to the measured results, those exceeded the 10 ng/g limit of lindane were aerial parts of cauliflower from both sites and violet from site B. Therefore, bioaccumulation of DDXs and HCHs in edible parts of vegetables from the area is still of concern after many years of inhibition of agricultural application. Relationship of HCHs and DDXs Levels between the Rhizosphere Soil and Vegetable Roots. The relationship between root and rhizosphere concentrations of individual vegetables is illustrated by plotting the former against the later in Figure 1 for the two sites separately. The concentrations are plotted in log scale to customize their log-normal distribution. Vegetable roots accumulate HCHs and DDXs directly from the rhizosphere soil, so a good correlation was expected between them. Except for the γ-HCH at both sites and δ-HCH at site A, linear correlation can be recognized between the roots and the rhizosphere soil for most compounds. Pearson correlation coefficients were significant at levels of less than 0.00009 and 0.0000006 for sites A and B, respectively. The deviations of γ-HCH and δ-HCH from the linear correlation may contribute to relatively high water solubility and bioavailability (31-33). Figure 2 illustrates the bioconcentration factors (BCFs) of total HCHs and DDXs for various vegetables. Although BCFs are generally given for bulk soil concentrations, they were calculated as root/rhizosphere soil concentration ratios in this study to emphasize the fact that roots directly contact with rhizosphere soil rather than bulk soil. Although the accumulation may not necessarily reached its equilibrium, the calculated BCF values still indicate the different tendencies of vegetable roots for absorbing HCHs and DDXs from the soil.
A two-way Anova was conducted with two hypotheses for BCFs: (1) no significant difference among the eight vegetable species; (2) no significant difference between the two sites. Both hypotheses were rejected at a level of 0.0001. In fact, except for carrot HCHs and cauliflower DDXs, the BCFs values at site B were always higher than those at site A. The significant difference of BCFs between the two sites may be explained by the following reasons: (1) Relatively high concentration of DOM at site B (Table 1) facilitated the mobilization of HCHs and DDXs in the soil. (2) The pesticide residuals at site B were fresher than those at site A, as suggested by the DDT/ DDE ratios previously discussed. It is often reported in the literature that toxic chemicals residing in soil become less bioavailable with time (34,35).
FIGURE 1. Relationship of the log-transformed concentrations of HCHs and DDXs between vegetable roots and the rhizosphere soils. VOL. 39, NO. 8, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Bioconcentration factors of HCHs (BCFHCH) and DDXs (BCFDDX) of roots over rhizosphere soil for various vegetables (from left to right: Cab, cabbage; Spi, spinach; Cau, cauliflower; Vio, violet; Cel, celery; Mus, mustard; Car, carrot; Tur, turnip) from the two sites. Significant differences in BCFs among the vegetable species studied can also be seen in Figure 2, implying a species-dependent uptake of HCHs and DDXs by vegetable roots. After the two-way Anova, a multiple comparison using Tukey HSD method was conducted. The resulting homogeneous groups (significant level of 0.05) of various vegetables in terms of BCF values are presented in Table 4. For comparison, the same test was performed for root and rhizosphere concentrations that were also significant based on the results of the two-way Anova. The orders of BCFs and root concentrations of various vegetables were very similar, though not identical, but very different from that of rhizosphere soil, leading to the broken lines in Table 4 for rhizosphere homogeneous groups. According to the results shown in Table 4, the most significant difference in both BCFs and root concentrations for total HCHs and DDXs is between the tuberous (mustard, turnip, and carrot) and fibrous (all others) root vegetables. The low concentrations in the tuber vegetable roots may be caused by the combination of two facts: (1) weak rootinduced mobilization activities in the rhizosphere soil, and (2) relatively small specific root surface area for uptake. There were also differences among various fibrous vegetables. Further study is necessary to reveal the reasons for such differences. For all the vegetable species from both sites, the mean concentration of total HCHs is much lower than that of total DDXs, while the root concentrations were similar to each other, resulting in much higher root BCFs of HCHs (2.64 ( 0.44) than DDXs (0.39 ( 0.07). It appears that vegetable roots absorb HCHs more effectively than DDXs. Miglioranza et al. also reported that carrots accumulate lindane from soil more efficiently than DDTs (36).
Acknowledgments Funding was provided by NSFC (Grant 40332015), National Basic Research Program (2003CB415004), NSFC (Grant 40021101), and Ministry of Science and Technology (Grant 2002BA906A76).
Literature Cited (1) Chen, S. P.; Chen, Z. W. Atlas of Environ. Qual. Tianjin; Sci. Press: Beijing, 1986. 2498
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Received for review July 18, 2004. Revised manuscript received October 31, 2004. Accepted December 6, 2004. ES048885S
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