Spatial Distribution and Enantiomeric Signatures - ACS Publications

Sep 24, 2014 - Program of Environmental Science, University of Houston-Clear Lake, Houston, Texas 77058, United States. •S Supporting Information...
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Hexachlorocyclohexanes in Tree Bark across Chinese Agricultural Regions: Spatial Distribution and Enantiomeric Signatures Lili Niu,†,‡ Chao Xu,§ Yang Xu,† Chunlong Zhang,∥ and Weiping Liu*,†,‡ †

International Joint Research Center for Persistent Toxic Substances (IJRC-PTS), MOE Key Laboratory of Environmental Remediation and Ecosystem Health, College of Environmental and Resource Sciences and ‡Research Center for Air Pollution and Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China § IJRC-PTS, College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou 310032, China ∥ Program of Environmental Science, University of Houston-Clear Lake, Houston, Texas 77058, United States S Supporting Information *

ABSTRACT: The environmental issue caused by atmospheric hexachlorocyclohexanes (HCHs) has been a worldwide concern due to their long-range transport potential. Tree bark is an excellent passive sampler for monitoring atmospheric pollutants. In this study, bark samples from agricultural regions across China were collected and analyzed to elucidate the contamination status of atmospheric HCHs and the enantiomeric composition of chiral α-HCH. Average contents of αHCH, β-HCH, γ-HCH, δ-HCH, and ∑HCHs in bark were 1.16, 2.51, 1.67, 0.368, and 5.71 ng/g (dry basis), respectively. Jing-Jin-Tang region was identified as the “hot-spot” of bark HCHs in China. Their residues were likely from the combined sources of historical applications of technical HCHs and lindane through long-distance transport. HCH contents were found inversely correlated with annual precipitation and temperature, but positively correlated with PM10 or PM2.5 due to the bioaccumulation of both vapor- and particle-phase HCHs by tree bark. Most bark samples preferentially accumulated (+)-αHCH, and the enantiomeric fractions (EFs) of α-HCH were positively correlated with α-HCH concentrations and the elevations of sampling locations. Compared to atmospheric analysis, tree bark analysis and enantiomeric signatures provide valuable timeintegrated information on the spatial distribution and transport pathways of atmospheric HCHs on the national scale in China.

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hydrocarbons (PAHs), brominated and chlorinated flame retardants, polychlorinated biphenyls (PCBs), and organochlorine pesticides (OCPs).4,6,8,11,12 Although there are several routes leading to POP accumulation in vegetation, it has been demonstrated that the primary pathway of POPs in tree bark is atmospheric deposition, except for trees grown directly in heavily contaminated soils.6,11,13,14 Therefore, the spatial patterns and sources of atmospheric pollution could be effectively monitored by tree bark.11 In addition, the collection of tree bark samples is less expensive, faster, and easier than conventional active and other sorbent-based passive air samplers, especially at remote locations.11 Because of the high lipid content and large surface area, tree bark can simultaneously trap vapor- and particle-phase POPs from the surrounding atmosphere.8 It can also accumulate these contaminants over a period of several years or longer, and

INTRODUCTION The pollution of persistent organic pollutants (POPs) is a critical environmental issue with serious worldwide concern due to their persistence, bioaccumulation, biomagnification, and toxicity in the environment. Hexachlorocyclohexanes (HCHs), one class of POPs recognized in 2009, were extensively applied as insecticides around the world during the 1950s to 1980s.1 Agricultural regions receiving the largest input of HCHs are the primary sources of HCHs.2,3 After reemission, HCHs underwent a long-range atmospheric transport, resulting in high detection frequencies in various environmental media far from their sources.2,4−7 Numerous factors play important roles in the global redistribution and fate of POPs in the air, including the physicochemical properties of the pollutants, rainfall, ambient temperature, particulate, wind, and so forth.2,3,8,9 Among the different HCHs, α-HCH is the only chiral isomer having two enantiomers. The enantiomeric profiles of α-HCH could be changed with various sources and sinks upon its deposition. Therefore, its enantioselective property can be advantageous for us to trace the transport and fate pathways of HCHs.3,7,10 Tree bark has been successfully used as a natural passive sampler for atmospheric POPs, such as polycyclic aromatic © XXXX American Chemical Society

Received: July 12, 2014 Revised: September 5, 2014 Accepted: September 24, 2014

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PCB 209. The extract was concentrated and exchanged into hexane. It was then transferred into a glass centrifuge tube and treated with concentrated H2SO4. After centrifugation, the organic layer was separated and the acid residue was back extracted with hexane twice. The combined organic layers were concentrated again and fractionated on a column containing Na2SO4, aluminum, and Na2SO4 from bottom to top. The column was eluted with 10 mL of hexane and 70 mL of hexane/DCM (7:3, v/v). The latter eluate containing target analytes was then concentrated and solvent-exchanged into hexane. Finally, the solution was reduced to 0.5 mL under a gentle N2 flow. The quantitative determination of HCHs was performed on a gas chromatograph (Agilent 7890A) equipped with a 63Ni electron capture detector. In addition, an Agilent 7890A GC5975C inert mass spectrometer was employed for the enantiomeric analysis of chiral α-HCH. Detailed operation conditions of instruments and columns for HCH analysis were described in our previous study.2 To determine the lipid contents in tree bark, a portion of the bark sample was ultrasonically extracted with hexane/acetone (1:1, v/v) three times. The filtrates were combined and evaporated at room temperature to a constant weight. Then the lipid concentration was gravimetrically measured before and after drying. Environmental Parameters. The elevations of sampling sites were simultaneously measured at the time of sampling. Meteorological parameters, including annual average temperature and precipitation, were collected from China Statistical Yearbook.17 In addition, the annual mean data of PM10 (N = 29) and PM2.5 (N = 45) were provided by China Statistical Yearbook and the report of Greenpeace, respectively.17,18 Quality Assurance and Quality Control. Strict quality control criteria were complied with to achieve correct identification and quantitation of HCHs during all analytical procedures. Glass apparatuses were cleaned and heated at 400 °C overnight before use. Procedural blank samples were used with every 15 bark samples to check the potential interference and contamination. The limits of detection (LOD) were determined as three times the signal-to-noise ratio. The calculated LOD values of the different HCH isomers were in the range of 0.02−0.06 ng/g. The recoveries of HCH isomers in spiked samples ranged from 83.1 to 112%. Surrogate standards were added in all samples to monitor the recoveries, which were 93.9 ± 12% and 89.2 ± 15% for TCmX and PCB209, respectively. Duplicate samples were used during extraction and analysis. Directly measured concentrations were reported in this paper without blank or recovery corrections. Enantiomeric fraction (EF), defined as the peak areas of (+)-α-HCH to that of the racemic α-HCH, was employed to present the results of chiral signatures. To ensure the reproducibility of enantiomeric analysis, racemic α-HCH standards were injected every 10 samples. Data were considered acceptable only when EF differences between the two monitored ions were within 0.05. In general, the standard EF value of α-HCH was 0.500 ± 0.005. Therefore, α-HCH in samples would be considered as racemic when the EF value was in the range of 0.496−0.504 (95% confidence interval) and vice versa. Statistical Analysis. The spatial distributions of HCH in tree bark across Chinese agricultural regions were depicted by the mapping software of geographic information system (GIS) (ArcGIS 9.3, ESRI, Redlands, California). Kriging method was

can thus be commonly employed for time-integrated monitoring of POPs on a regional or global scale.15 Several studies have been conducted in China to monitor the HCH pollution in tree bark.4,8,12 The total and individual isomers of HCHs in bark were determined in the western parts of China to reveal the geographic distributions and transport of HCHs in the atmosphere.4,12 The total OCP concentrations in bark from urban areas across China were also reported by Zhao et al.8 However, no nationwide monitoring of bark samples has been conducted to date to map the extent of atmospheric HCH concentrations in rural areas in China, or the enantiomeric compositions of chiral α-HCH. Therefore, tree bark samples from agricultural fields across China were collected in this study to analyze the residues of HCHs. We aimed to shed light on (a) the spatial distribution and transport patterns of atmospheric HCHs, (b) the influence of environmental conditions on HCH distribution, and (c) enantiomeric signatures of α-HCH in rural tree bark. The results from this study may provide baseline information on the status of HCHs in tree bark and thus fill the data gap concerning their transport and fate pathways in the air after the ban of HCHs in China. To the best of our knowledge, this is the first study on the national monitoring of atmospheric HCHs through tree bark and enantiomeric signatures of αHCH in rural regions in China.

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MATERIALS AND METHODS Sample Collection. A total of 121 tree bark samples were collected from rural areas of 30 provinces, municipalities, and autonomous regions in four large geographic regions across China, i.e., Northeast, East, West, and Central China, in April and May 2013. All sampling sites were adjacent to agricultural fields and located by global positioning system (GPS). A detailed distribution of the sampling locations is shown in Figure S1 of the Supporting Information (SI). The unified standard operating procedures were followed throughout the whole bark sampling process. Trees such as pine, poplar, camphor, and fir were chosen as the preferred species due to their wide geographical distributions in China. At each sampling location, tree bark samples were collected at the height of 1.5 m from 3−7 individual trees with ages of approximately 15−20 years (trunk diameter 20−30 cm). Trees with moss and lichen on the surface were excluded from sampling. The sampling thickness of bark was within 2 mm, which is sufficient for the analysis of residual pollutants while protecting trees from being permanently harmed.16 Bark from four different sides of each tree was cut off using a precleaned stainless steel sickle and combined to one sample in a precleaned aluminum foil bag. The tree bark samples were then immediately shipped to the laboratory at Zhejiang University and kept at −20 °C until analysis. Sample Extraction and Analysis. The analytical standard mixtures of HCHs and surrogates were obtained from AccuStandard Inc. (New Haven, CT, USA). All other solvents and reagents used were of residue analysis grade and purchased from J&K Chemical Ltd. (Beijing, China). Anhydrous granular sodium sulfate (Na2SO4) and aluminum were activated before use. Tree bark samples were freeze-dried, cut into small pieces, and ground before extraction. The procedures modified from Zhao et al.8 were employed to extract HCHs from bark samples. In brief, a portion of bark containing Na2SO4 was Soxhlet extracted using hexane/dichloromethane (DCM) (1:1, v/v) after being spiked with surrogate standards TCmX and B

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HCH concentrations observed by Yang et al. and He et al., whereas the elevated concentrations of α-HCH in bark in European countries might be the direct results of trees grown in a heavily polluted area.4,12,16 For a better insight into the regional variations of HCHs in rural tree bark across China, GIS and Kriging spatial interpolation method were employed to map their spatial distributions (Figure 1). The highest levels of HCH residues, which averaged 76.2 ng/g tree bark, were observed in Tianjin, China. Such surprisingly elevated concentrations of HCHs might be related to the large amounts of historical HCH usage and the emissions from several major pesticide plants in the areas.8 In addition, Beijing City and Shanxi, Shannxi, Hebei, and Liaoning provinces, where bark concentrations of HCHs exceeded 6.9 ng/g, were also identified as the “hot-spots”. This is consistent with Zhao et al., who also found elevated OCPs (sum of α-, β-, γ-, δ-HCH, and HCB) concentrations in bark at urban sites in Tianjin, Shanxi, and Hebei provinces due to the extensive use of HCHs in the past.8 Furthermore, it has been demonstrated that the concentrations of organochlorine pesticides in the air corresponded well to socioeconomic indicators.20,21 Interestingly, the “hot-spots” of bark HCHs identified in this study are where the Jing-Jin-Tang region in China is located. It represents a region with rampant development of agriculture and urbanization in the past decades. Therefore, the highest residues found in these sites could be partially attributed to the HCH usage associated with the fast economic development in this region. In general, the contamination of atmospheric HCHs was the most serious in East China, followed by Northeast, Central, and West China (SI Table S2). For α- and γ-HCHs, elevated concentrations were also found in West China besides Jing-Jin-Tang region. Their presence in these remote regions can only be explained by the secondary sources through long-distance transport. Composition Profiles of HCHs in Tree Bark. The composition profiles of HCH isomers in rural tree bark from each province are shown in Figure 2. Overall, β-HCH was the dominant isomer in most samples across China, contributing from 15.1 to 86.2% to the total HCHs in tree bark. Similar isomer profiles of HCHs in tree bark were also reported by Tarcau et al. and He et al.6,12 The predominance of γ-HCH was found in Shanghai City and Jiangxi, Shandong, Yunnan, Henan, Guangxi, Tibet, Hainan, and Heilongjiang provinces, with a range from 35.5 to 62.5%. In addition, Hunan and Xinjiang provinces were dominated by α-HCH. In general, the fractions of α-HCH and γ-HCH were the highest in West China, while β-HCH and δ-HCH were the highest in Northeast and East China, respectively (SI Table S2). The diverse composition profiles of HCHs in bark across China are not unexpected because of the different dissipation rates of theses HCH isomers with inherently different physicochemical properties and environmental conditions at different sites. By comparison with the composition of a technical mixture of HCHs (60−70% α-HCH, 5−12% β-HCH, 10−12% γ-HCH, 6−10% δ-HCH, and 3−4% ε-HCH),22 the ratios of HCH isomers can be used to deduce the origins, ages and transport pathways of HCH residues in tree bark across China. The ratio of α-HCH/γ-HCH ranges from 4.64−5.83 and that of αHCH/β-HCH is approximately 11.8 in technical HCH. In addition, lindane is composed of 99.0% γ-HCH and thus the ratio of α-HCH/γ-HCH from lindane is nearly zero. After being released into the environment, the α-HCH/γ-HCH ratio in technical HCHs would increase due to the longer

utilized for the interpolation of HCH levels in tree bark between locations. The linear regression analyses of HCH concentrations and EFs of α-HCH in tree bark versus meteorological conditions and other environmental parameters were performed using Origin software (OriginLab Corp., Northampton, MA, USA).

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RESULTS AND DISCUSSION Spatial Distribution of Bark HCH Concentrations in Chinese Agricultural Regions. On the basis of trunk diameter in the range of 20−30 cm, we could deduce that the age of these trees was approximately 15−20 years.8 The tree bark samples therefore had similar time of exposure to HCHs. In addition, since the usage of HCHs has been forbidden for 30 years in China, equilibrium can be assumed for the HCH partitioning between bark and air. Therefore, tree bark can indicate a historical contamination of HCHs in the air of China. The summary statistics of total and individual HCH concentrations in tree bark from rural areas across China are tabulated in Table 1. The residues of total HCHs were detected Table 1. Descriptive Statistical Summary of HCH Concentrations in Tree Bark across China (ng/g, Tree Bark) mean median min max SDb CV (%)c DF (%)d

α-HCH

β-HCH

γ-HCH

δ-HCH

∑HCHs

1.16 0.965 BDLa 16.6 1.50 129 98.3

2.51 1.32 0.274 73.2 6.97 277 100

1.67 1.28 BDLa 20.2 1.88 113 97.5

0.368 BDLa BDLa 17.3 1.76 478 13.2

5.71 3.74 1.38 127 11.7 205 100

a

BDL: below detection limit. bSD: standard deviation. cCV: coefficient of variation. dDF: detection frequency.

in all samples, implying the ubiquitous pollution of HCHs in China. In terms of HCH isomers, the detection frequencies of α-HCH, β-HCH, γ-HCH, and δ-HCH were 98.3, 100, 97.5, and 13.2%, respectively. The coefficients of variations were from 113 to 478%, indicating a large variability of HCH residues due to the large sampling area in this study. The total concentrations of HCHs ranged from 1.38 to 127 ng/g tree bark, with a mean of 5.71 ng/g. Among the HCH isomers analyzed, β-HCH was the most abundant isomer in tree bark (range 0.274−73.2 ng/g) based on its mean concentration of 2.51 ng/g (Table 1). This ubiquitousness might be attributable to its higher stability and stronger bioaccumulation potential compared to other isomers.6 Similar to He et al.,12 the levels of other isomers in tree bark were in the order of γ-HCH > αHCH > δ-HCH, with concentrations ranging from below detection limit (BDL) to 20.2, BDL to 16.6, and BDL to 17.3 ng/g, respectively. The lipid contents of up to 9.48% in tree bark samples, which were relatively higher than other forms of vegetation, support the claim that tree bark could serve as an effective passive sampler for hydrophobic pollutants. A comparison of HCH concentrations in tree bark found in this and other studies is given in Table S1 of the SI. Overall, the contents of HCHs in tree bark presented in this study were medium relative to those in the reported studies. They were lower than those determined in Moldavia, Romania, and some European countries,6,16 while higher than those reported by Olivella et al., Yang et al., and He et al.4,12,19 The remote tree bark sampling sites might be the main explanation for the lower C

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Figure 1. Spatial distribution of individual and total HCH concentrations in rural tree bark across China. BDL: below detection limit.

atmospheric lifetime of α-HCH than γ-HCH (120 versus 96 d) and the photoisomerization of γ-HCH to α-HCH.23,24 In contrast, the ratio of α-HCH/β-HCH would decrease over time because of the isomerization of α-HCH and γ-HCH to βHCH.23,25 In this study, the ratios of α-HCH/β-HCH in all bark samples were found to be far lower than 11.8 (SI Figure S2a). The elevated proportion of β-HCH suggests that the HCH residues in Chinese tree bark were mainly from the past usage. This result was further confirmed by the correlations between the total and individual HCH concentrations in tree bark (SI Table S3). Significant correlations were observed among these isomers (P < 0.01), indicating their similar

historical sources. In addition, the highest correlation was observed between β-HCH and ∑HCHs (R = 0.904) likely due to the most stable nature of β-HCH. The ratios of α-HCH/γHCH in tree bark were all lower than 4.64, decreasing with the increasing elevations of sampling sites (SI Figure S2a, b). These results showed that the time-integrated HCHs in tree bark over the decades could well reflect the historical pollution of HCHs. Given that lindane with low α-HCH/γ-HCH ratio was continuously being used until 2000 after the ban of technical HCH in China,26 the low α-HCH/γ-HCH isomer ratios observed in this study therefore indicates the additional source from lindane. A similar pattern of recent lindane input was also D

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Figure 2. Relative abundance of HCH isomers in tree bark across Chinese agricultural regions.

temperatures and higher elevations.31,32 Davidson et al. collected various conifer needles from mountain areas of Alberta and British Columbia and found a strong temperature dependence of α-HCH concentrations.33 Wang et al. also observed an increased level of HCHs in Himalayan spruce needles from sites with higher elevations (lower temperatures).29 A similar trend of HCHs in vegetation samples along temperature variations was also reported in southeast Tibetan Plateau.34 Likewise, a significant negative correlation (R = −0.316, P < 0.001) between ∑HCHs levels and annual average temperature was also found in this study. These results highlight that temperature is a key factor influencing the redistribution of HCHs in the air over the past 15−20 years. The temperature dependency is associated with the “cold condensation” of volatile HCHs that are prone to condense at regions with lower temperatures. In addition, the differential air-bark partitioning at different temperatures over the year at the same site might partly contribute to the extreme variability as shown in Figure 3a. As mentioned above, the “hot-spot” of tree bark HCHs was identified in Jing-Jin-Tang district in China. Interestingly, this site is also one of the regions with severe haze pollution in China in recent years.35 Given that tree bark can accumulate pollutants from both vapor and particle phases, the dependence of ∑HCHs concentrations in tree bark on the levels of particulate matter (PM) warrants further analysis. Significant positive correlations were observed between the total concentrations of HCHs and PM2.5 (R = 0.376, P = 0.010) or PM10 (R = 0.367, P = 0.050) (Figure 3b). The regression of ∑HCHs concentrations against PM10 is somewhat weaker and less significant than PM2.5. This agrees well with our general recognition that the adsorption to finer PM is much stronger, due to its larger surface area, than adsorption to the coarser PM. It is also well-known that the fine particulates in the atmosphere mainly originated from anthropogenic activities.36

identified in tree bark by Yang et al., Tarcau et al., and He et al.4,6,12 In addition, the sites with high elevations are mostly located in the west part of China. They are adjacent to countries, such as India, Bangladesh, and Nepal, where lindane is continuously being manufactured and used.27,28 Therefore, the new input of lindane from surrounding countries via longrange transport could be another reason for the low α-HCH/γHCH ratios at high-elevation sites in West China.4 The decreasing α-HCH/γ-HCH with increased elevation gradient was also observed in spruce needle by Wang et al.29 In this earlier study, the cause for the higher ratio of α-HCH/γ-HCH in low elevation mountain sites was deduced to be the new source of α-HCH. In contrast, a positive correlation with elevation was found by Yang et al., who suggested that the older or more distant sources of HCHs might become primarily responsible for this relationship.4 Influence of Environmental Conditions. The global usage of technical HCHs has been phased out for several decades; therefore, their distributions in the air are mainly governed by the reemission of HCHs (secondary sources) over primary sources of technical HCHs. Wet deposition has been suggested as a particularly effective transport mechanism influencing HCH redistribution in the environment due to the relatively high water solubility of HCHs.2,30 As expected, in this study, HCH concentrations in tree bark were found significantly negatively correlated with annual precipitation data with R = −0.349 (P < 0.0001) after omitting an outlier from Tianjin (Figure 3a). This negative correlation can be explained by the dissipation of HCHs from the air by wet deposition over a long period of time. The concentration of HCHs in Tianjin was considered as an outlier because of its exceedingly high zscore of 10.4 (z ≫ 3). It has been demonstrated that the accumulation of POPs in the environment, especially the more volatile ones, could be enhanced through global distillation effect at sites with lower E

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into inferring the sources, ages, and fate pathways over long distances due to their stereoselective degradation in the chiral environment.10,39,40 Chiral compounds from primary sources are expected to be racemic or close to racemic, while those from secondary sources are typically nonracemic following enantiomeric dissipation.41,42 Because only α-HCH is chiral with two enantiomers, the enantiomeric signature of α-HCH in the air would be retained when they are affected by the volatile nonracemic residues.41,42 The enantioselective accumulation of α-HCH has been observed in various environmental compartments, such as air, water, soil, and vegetation.2,6,43 In this study, the EF values of α-HCH in tree bark varied in a wide range from 0.143 to 0.995, with an average value of 0.655. Most bark samples showed EF values deviating from 0.5, indicating the past use of HCHs in these sites. Similar nonracemic α-HCH signatures were also observed in the air in Romania, Europe, the Great Lakes, and the Arctic.6,42,43 In addition, there were 81% of the bark samples showing a preferential depletion of (−)-α-HCH (EF > 0.5), which agrees with those in tree bark collected in Romania.6 Preferential accumulation of (+)-enantiomer was observed at sites with elevated lipid-normalized αHCH concentrations (SI Figure S3a). Results obtained were observed by Zhang et al. in that the lowest EFs were found at the sites with the highest concentrations of α-HCH.44 It is likely that certain stereoselective degrading microbes may be stimulated at high concentrations of α-HCH. Because numerous studies revealed that the EFs in the air were mainly impacted by secondary sources from soil and water, the EFs of α-HCH in tree bark were compared with those in soils previously reported.2,10,43 We found that the EF values of α-HCH in both tree bark and soils from agricultural fields were mostly higher than 0.5 and the (+)-α-HCH was preferentially accumulated at sites with elevated α-HCH concentrations. Although there are several pathways for organic pollutants to reach tree bark, their indirect uptake from soil contributes very little and the atmospheric deposition was shown to be the primary pathway for the accumulation of organic pollutants in tree bark.6,45 In addition, because the 2mm thick bark samples were primarily dry dead tissue composed of keratinized cells in the outermost tree, the microbial population in bark should be very small. Therefore, the enantiomeric signatures of α-HCH in rural tree bark should be mainly impacted by their long-period volatilization from soils and the subsequent wet or dry deposition, rather than intake by root or enantioselective degradation by microbes in bark. In contrast, racemic or nearly racemic enantiomeric signatures of α-HCH were observed in inland air samples, which suggested a possible recent input of HCHs.43 SI Figure S3b shows a significantly increased EF value (P = 0.037) with increasing sampling elevation. This suggests a selective depletion of (−)-α-HCH in tree bark from sites with higher elevations. Our results differ from those of a previous study by Covaci et al.43 who observed a negative correlation between EFs of α-HCH in the air and temperature. The discrepancies can be explained by the diverse temperature-dependent microbes because of the temperature variations at different sites.46 Unlike the study of Tarcau et al., our results also revealed similar enantiomeric compositions among different tree species (data not shown), implying that the chiral selectivity of α-HCH by tree species was insignificant.6 Furthermore, this study utilized tree bark as a passive sampler to provide insight into the spatial distribution patterns and transport pathways of atmospheric HCHs. HCHs in tree bark

Figure 3. Correlations of the ∑HCH concentrations with (a) annual precipitation and temperature (the outlier observed in Tianjin was excluded from the analysis) and (b) PM10 (N = 29) and PM2.5 (N = 45). C: concentration; T: temperature; P: precipitation.

Therefore, the redistribution of HCHs in China might be facilitated by human activities as well. Most previous studies of the atmospheric organic pollutants commonly focused on the vapor-phase concentration due to its predominance in total levels.37,38 Our study in regard to a significant correlation between ∑HCHs concentrations and PM, however, suggests the involvement of particle phase in the overall transport of HCHs in the air, especially in the regions with heavy haze pollution. Our results imply that future studies on long-range transport of atmospheric pollutants should consider both the vapor- and particle-phase concentrations. Moreover, tree bark can be used as an excellent natural passive sampler for atmospheric pollutants, as was supported by other studies. For instance, Salamova and Hites found a higher correlation between bark with combined vapor and particle-phase atmospheric pollutant concentrations than those in a single phase, highlighting the accumulation of both vapor and particle phases by tree bark.15 Tarcau et al. observed that the accumulation of OCPs in tree bark was mainly through dry deposition and influenced by air particles.6 A similar conclusion was also drawn by Zhao et al., who reported a more pronounced accumulation of particle-bound PAHs into the barks, especially at the bark surface, than the gaseous PAHs.9 Enantiomeric Signatures of Chiral α-HCH. For chiral chemicals, enantiomeric analysis can provide further insight F

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showed a correlation with atmospheric PM, suggesting the important role of particulate-bound HCHs in the overall transport and fate processes. With the increasingly severe haze episodes in China in recent years, the potential risks induced by inhalable particles and particulate-bound contaminants are of great public concern. Overall, our integrated approach using HCH concentrations and enantiomeric levels in tree bark, along with vapor- and particle-phase pollutants, warrants further research for a full account of the health risks related to HCHs and other POPs in the atmosphere.

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ASSOCIATED CONTENT

* Supporting Information S

Detailed information on sampling sites across China, comparison of HCH concentrations in tree bark between this and other studies, summary of HCH concentrations and isomer fractions in bark from four geographic regions of China, and relationships among HCH isomers. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: +86-571-8898-2341; fax: +86-571-8898-2341; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was funded in the part by the National Natural Science Foundation of China (21177112, 21320102007), and the Ph.D. Programs Foundation of the Ministry of Education of China (20120101110132). We thank Drs. Yuezhong Wen and Fangxing Yang, and Mr. Wanpeng Liu, Zhisheng Zhang, and Jinjian Ding for their assistance in sample collection.

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