Residues, spatial distribution and risk assessment of DDTs and HCHs in agricultural soil and crops from the Tibetan Plateau

Chemosphere 149 (2016) 358e365

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Residues, spatial distribution and risk assessment of DDTs and HCHs in agricultural soil and crops from the Tibetan Plateau Chuanfei Wang a, Xiaoping Wang a, b, *, Ping Gong a, b, Tandong Yao a, b a

Key Laboratory of Tibetan Environment Changes and Land Surface Processes, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, 100101, China b CAS Center for Excellence in Tibetan Plateau Earth Sciences, China

h i g h l i g h t s
Levels of OCPs in the Tibetan farmland were relatively low in a global perspective.
OCPs in the Tibetan agricultural soil were from historical residues.
OCPs in the crops mainly came from fresh input via atmospheric deposition.
OCPs in Tibetan farmland will not pose non-cancer and cancer risks to the residents.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 11 November 2015 Received in revised form 27 January 2016 Accepted 29 January 2016 Available online xxx

Due to its high elevation and cold temperature, the Tibetan Plateau (TP) is regarded as the “Third Pole”. Different from other polar regions, which are truly remote, the TP has a small population and a few agricultural activities. In this study, agricultural soil and crop samples (including highland barley and rape) were collected in the main farmland of the TP to obtain the contamination levels of dichlorodiphenyltrichloroethane (DDT) and hexachlorocyclohexane (HCH) in the Tibetan agricultural system as well as the relevant human exposure risks. The average concentrations of DDTs and HCHs in the agricultural soil, highland barley and rape were 1.36, 0.661, 1.03 ng/g dw and 0.349, 0.0364, 0.0225 ng/g dw, respectively. In the agricultural soil, DDTs and HCHs matabolism (DDE, DDD and b-HCH) were abundant, which indicated a “historical” source, whereas crops contained a similar composition ((DDE þ DDD)/DDT, a/b-HCH and a/g-HCH) to that of wild plants, suggesting that the DDTs and HCHs in crops are likely from long range atmospheric transport. The human health risks via non-dietary and dietary to DDTs and HCHs in the farmland were assessed. All of the hazard index (HI) values of DDTs and HCHs for non-carcinogenic risks were <1, and most of the cancer risk values were <106, suggesting that DDTs and HCHs in the farmland will not pose non-carcinogenic risks and will pose only very low cancer risks to the Tibetan residents. © 2016 Elsevier Ltd. All rights reserved.

Handling Editor: Keith Maruya Keywords: DDTs HCHs Agricultural soil Crops Health risk assessment Tibetan plateau (TP)

1. Introduction For controlling pests and diseases effectively, dichlorodiphenyltrichloroethane (DDT) and hexachlorocyclohexane (HCH) were used widely between the 1940s and the 1980s (Simonich and Hites, 1995). However, application of these organochlorine pesticides (OCPs) resulted in adverse environmental and health

* Corresponding author. Key Laboratory of Tibetan Environment Changes and Land Surface Processes, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing, 100101, China. E-mail address: [email protected] (X. Wang). http://dx.doi.org/10.1016/j.chemosphere.2016.01.120 0045-6535/© 2016 Elsevier Ltd. All rights reserved.

consequences (Abhilash and Singh, 2009; Czub and McLachlan, 2004; Simonich and Hites, 1995; Tao et al., 2009). In this case, the Stockholm Convention (2001) has terminated the agricultural use of DDT and HCH but only allows DDT use for malaria disease control. Although the prohibition for agricultural use has continued for decades of years, the residues of pesticide in the soil and food can cause acute or chronic health problems to humans (Mekonen et al., 2015). The soil system has a large retention capacity for hydrophobic compounds and has been identified as a location for the long-term storage of DDTs and HCHs (Nam et al., 2008). However, with the temperature rising, the semi-volatile OCPs in soil will be re-

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volatized and dispersed (Tao et al., 2008; Wong et al., 2008). For example, in India, the volatilization of OCPs from the soil occurred in cities having higher ambient temperatures (Chakraborty et al., 2015). Hence, the soil system may become a second source of OCPs, especially for tropical and agricultural soil (Bidleman and Leone, 2004; Chakraborty et al., 2015; Wong et al., 2008). Due to being affected by the regular turning up of agricultural soil, the exchange of volatile chemicals among soil, air and plants was accelerated (Bidleman and Leone, 2004; Komprda et al., 2013; Waliszewski et al., 2008). The crops possibly absorbed OCPs from the soil through their roots and captured the suspended particulate- and gas-phase OCPs from contaminated soil through their leaves (Lin et al., 2007; Tao et al., 2005). Generally, OCPs were detected in various grains and vegetables, such as wheat, rice, maize, cabbage and carrots (Guler et al., 2010; Mahmood et al., 2014; Mekonen et al., 2015; Tao et al., 2005). It was estimated that agricultural food accounted for nearly 35% of the daily intake of OCPs by human beings in Hong Kong (Chung et al., 2008). Therefore, residual OCPs in farmland are doomed to arouse potential health risks to the residents, especially for the agricultural regions in the highlands where the OCP concentrations were often higher than those in the plains (Niu et al., 2013; Zhang et al., 2011). The Tibetan Plateau (TP) is the highest plateau in the world. The environment of the TP is generally clean similar to the Arctic (Huang et al., 2012; Jia et al., 2014; Xiao et al., 2012). Given the TP approaches the Indian subcontinent, the persistent organic pollutants (POPs) in this region mainly come from long-range atmospheric transport (LRAT). Previous studies supported the view that OCPs and black carbon in the TP environment can come from the Indian subcontinent as driven by the Indian Monsoon (Cong et al., 2015; Kaspari et al., 2011; Ren et al., 2014; Xu et al., 2009). Additionally, Wang et al. (2012) studied OCPs in the no-agricultural soil across the TP and found higher concentrations of OCPs were detected in the southeastern TP. On the other hand, there are a few agricultural activities that occur in the TP. Based on a short monitoring time in Lhasa, the capital city of the TP, higher concentrations of atmospheric OCPs were detected, which were attributed to possible local emission (Gong et al., 2010; Li et al., 2008). Currently, knowledge regarding the agricultural use of OCPs in the TP is absent, resulting in a hazy understanding of the actual level of OCPs in the farmland of the TP. Carrying out work on the farmland where pesticides were probably used is essential to determining the local contribution of OCPs in the TP. The aims of the present study were to investigate (i) the levels of DDTs and HCHs in the agricultural soil and crops; (ii) the spatial distribution of DDTs and HCHs in different agricultural regions of the TP; (iii) the possible sources of DDTs and HCHs (residual versus new input) and (iv) the health risks for the residents due to exposure to DDTs and HCHs in the farmland. 2. Materials and methods 2.1. Sampling sites The climate of the Plateau is cold and dry in the northwestern region, and it is warm and humid in the southeast (Wang et al., 2010). Influenced by the cold climate, the northern and western TP, including Agari and Naqu, are mixed farming and pastoral regions (Fig. 1). The agricultural zones are dominantly distributed in the southeast (warm and humid) regions, such as the city of Lhasa as well as the Xigatse, Shannan, Nyingchi and Qamdo prefectures (Fig. 1). The agricultural areas in the southeast account for approximately 96% of the total farmland in the TP (Agricultural geography of the Tibetan Plateau, 1984). In this study, 60 agricultural soil samples and 52 crop samples were collected in these

359

Fig. 1. Sampling sites from the agricultural regions of the Tibetan Plateau. Agricultural soil and crop samples were collected from the red sites on the map; only agricultural soil samples were collected from the yellow sites marked on the map. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

agricultural regions (Fig. 1). The crop species included highland barley (Hordeum vulgare Linn. var. nudum Hook. f.) and rape (Brassica campestris L.). In total, 47 highland barley samples and 5 rap samples were collected. The specific information regarding elevation, soil organic carbon (SOC), and species of crops for the sampling sites are given in the Supporting Information (SI) Table SI-1.

2.2. Sample collection The agricultural soil samples were taken far away from the roads in 2011. The samples were collected using a stainless steel handheld corer. The first two cores were always discarded. Three cores (0e5 cm) taken from an area of 100 m2 were combined together to form one sample. Crop samples were sampled as synchronously as possible at every sampling site. To avoid direct contamination from the surface soil, the bottoms of the crops with adhering soil particulates were cut off, and the aerial parts were collected. Five subsamples (one in the center and four in the corner) from the 100 m2 area constituted one crop sample. Both the agricultural soil and crop samples were wrapped in aluminum foil twice and sealed in two plastic bags to minimize the possibility of contamination. All of the agricultural soil and crop samples were stored at 20  C until extraction. The moisture contents of soil and crop samples were measured by comparing the fresh and dry weight (dw) measurements of the samples after oven drying 2 g of sample at 105  C for 15 min and 90  C for 24 h, respectively. The measured moisture contents were 13% ± 5% for soil and 37% ± 24% for the crops.

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2.3. Sample extraction and analysis

2.5. Health risk assessment

A 30 g wet agricultural soil sample mixed with 30 g of anhydrous sodium sulfate was Soxhlet extracted with 200 mL of dichloromethane (DCM) at 48  C for 16 h. Each sample was spiked with 2 ng of PCB-30 and Mirex as recovery surrogates. The extract was evaporated to 1 mL and solvent-exchanged by n-hexane in a rotary evaporator. The concentrated extract was loaded on the top of an aluminum/silica column (10 g activated alumina/9 g activated silica and 2 g anhydrous sodium sulfate) and eluted with 180 mL of a mixture of n-hexane and DCM (1:1 v/v). The elute was concentrated to 1 mL and further cleaned using gel permeation chromatography (GPC, containing 6 g of Biobeads SX 3) using 46 mL of a mixture of n-hexane and DCM (1:1 v/v). The first 16 mL was discarded, and the last 30 mL was collected. Then, the final volume was concentrated to 100 mL containing 2 ng of pentachloronitrobenzene (PCNB) and PCB-209 as internal standards under a gentle stream of high-purity nitrogen. The crop samples were first washed by deionized water to remove dust adhering to the leaves. Then, 20 g of fresh crop samples mixed with 30 g of anhydrous sodium were extracted. The extraction and cleaning process was similar with that mentioned above, but a process was added after cleaning by the aluminum/ silica column. To remove lipids and waxes, the sample was concentrated to 4 mL in n-hexane and shaken with approximately 1 mL of sulfuric acid. Then, the sample was further cleaned by GPC to remove any remaining lipids. The producer and grades of solvents and materials mentioned above are given in Text SI-1. All of the samples were analyzed by a gas chromatograph (GC) with an ion-trap mass spectrometer (MS) (Finnigan Trace GC/ PolarisQ) with a CP-Sil 8CB capillary column (50 m  0.25 mm  0.25 mm) operating under selective ion monitoring (SIM) mode. High-purity helium was used as the carrier gas at 1.0 mL/min. The temperature of injection port was 250  C and 1 mL of sample was injected. The oven temperature of the system began at 100  C for 2 min, increased to 140  C at 20  C/min, increased to 200  C at 4  C/min (held for 10 min), and then increased to 300  C at 4  C/min, where it was maintained for 17 min. The compounds detected include a, b, g, d-HCH, o,p0 -DDT, o,p0 -DDE, o,p0 -DDD, p,p0 -DDT, p,p0 -DDE and p,p0 -DDD. The SOC contents were measured using a total organic carbon (TOC) analyzer (Shimadzu 5000-A) with the solid sample module.

The DDTs and HCHs in the farmland will affect human health via two main pathways, namely non-dietary (ingestion, dermal contact, and inhalation of soil) and dietary (highland barley and rape grown in the agricultural soil were considered in this study) pathways. The risks of DDTs and HCHs in farmland of the TP were estimated according to the U.S. Environmental Protection Agency (EPA) Handbook in 1997 but some parameters were replaced by the local survey (Text SI-2). The exposure health risks to humans include non-carcinogenic and cancer risks. The average daily dose (ADD, mg/kg/day), hazard quotient (HQ) and hazard index (HI) are the primary indices to assess non-carcinogenic risks. The ADD of OCPs via non-dietary and dietary pathways is calculated by formulas offered in Text SI-2. The HQ is gained based on the ADD and the specific reference dose (RfD) (Text SI-2). The non-carcinogenic risks of a certain chemical through multiple exposure pathways are presented as the HI (Text SI-2). Details to calculate each parameter are given in Text SI-2. For each compound, if the HI > 1, it indicates that the risk is very high; if the HI < 1, it indicates that the risk does not exist (Man et al., 2011; Niu et al., 2013). The cancer risk is estimated by the ADD multiplied by each slope factor of individual exposure routes (Text SI-2). The cancer risks of one compound are assessed by the sum of the cancer risks from ingestion, dermal contact, inhalation and diet. The cancer risks are divided into 5 degrees. If the value of cancer risk <106, the risk is considered very low. The risk is low when the value is 106-104, moderate when it is 104-103, high when it is 103-101 and very high when it is > 101. The values of the parameters mentioned above are listed in Table SI-2.

2.4. Quality assurance and quality control (QA/QC) All analytical procedures were performed under strict quality assurance and control measures. Laboratory blanks for agricultural soil and crop samples (extraction of a thimble filled with anhydrous sodium sulfate) were included at a rate of one for every ten samples and were treated in exactly the same manner as the samples. However, most of the OCPs were not detected in the laboratory blanks, indicating contamination was negligible during analysis. In this case the concentration of the lowest calibration standard was taken as the limit of quantitation (LOQ). The LOQs for the DDTs and HCHs were between 0.01 and 0.1 pg/g based on 26 g dw soil samples and 0.01e0.2 pg/g based on 13 g dw crop samples. Recoveries were between 60% and 121% for PCB-30 and between 72% and 133% for Mirex in soil samples. For crop samples, the recoveries were 49e94% for PCB-30 and 54e79% for Mirex. All of the results were not corrected for the recovery rates. The non-detects were substituted with ½ LOQ in cases where greater than 70% of data were detected.

3. Results and discussion 3.1. Levels of DDTs and HCHs in agricultural soil and crops The DDTs and HCHs were detected in agricultural soil and crop samples in the TP. The full data sets for concentrations of OCPs in the agricultural soil, highland barley and rape are given in Tables SI3-5. The descriptive statistical data (including minimum, maximum, mean and standard deviation) of OCP concentrations in agricultural soil and crops of the TP are listed in Table 1. Comparison between the present study and other studies on the surface soil of the TP and farmland in other regions are presented in Table 2. The concentrations of DDTs and HCHs in the agricultural soil were in the range from below detection limit (BDL) to 41.6 and BDL-8.36 ng/g dw, respectively (Table 1), which were similar with those in Antarctic soil (0.52e3.68 ng/g dw for DDTs and 0.49e1.34 ng/g dw for HCHs, Klanova et al., 2008). The average concentrations of DDTs and HCHs were 1.36 ± 5.71 and 0.349 ± 1.22 ng/g dw, respectively, which were comparable to those in the remote soil of the TP (0.882 ng/g dw for DDTs and 0.226 ng/g dw for HCHs, Wang et al., 2012, Table 2). Compared with the agricultural soil in China (average values in the range: 21.4e152 ng/g dw for DDTs and 1.74e15.4 ng/g dw for HCHs), the concentrations of DDTs and HCHs in the Tibetan agricultural soil were generally lower (Gao et al., 2008; Jiang et al., 2009; Tao et al., 2005; Zhou et al., 2013) (Table 2). In the agricultural region of mainland China, the relatively higher temperatures throughout the year contribute to multiple growing seasons and more agricultural activities than in the TP. Compared with the agricultural soil in the other countries, the average concentrations of DDTs and HCHs in the Tibetan agricultural soil were approximately three orders of magnitude lower than those in India (903 and 825 ng/g dw for DDTs and HCHs, respectively, Mishra et al., 2012), the southern United States (211 ng/g dw for DDTs, Bidleman and Leone, 2004) and northwestern Spain

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Table 1 The descriptive statistical data (minimum, maximum, mean and standard deviation) of OCP concentrations (ng/g dw) in agricultural soil and crops of the TP. Soil

o,p'-DDE p,p'-DDE o,p'-DDD o,p'-DDT p,p'-DDT DDTs a-HCH b-HCH g-HCH d-HCH HCHs

Highland barley

Rape

Minimum

Maximum

Mean

SD

Minimum

Maximum

Mean

SD

Minimum

Maximum

Mean

SD

BDL BDL BDL BDL BDL BDL 0.0019 BDL BDL BDL BDL

0.0978 17.1 0.0918 4.56 21.3 41.6 0.265 7.76 0.153 0.189 8.36

0.0095 0.728 0.0292 0.305 6.65 1.36 0.0353 0.295 0.0203 0.0186 0.349

0.0187 2.63 0.0353 0.859 9.95 5.71 0.0499 1.17 0.0288 0.0340 1.22

BDL 0.0007 BDL 0.0037 0.0028 0.0071 BDL BDL BDL BDL BDL

0.0262 4.00 BDL 0.784 3.18 7.77 0.0601 0.147 0.0326 BDL 0.229

0.0082 0.181 e 0.123 0.351 0.661 0.0120 0.0174 0.0094 e 0.0364

0.0058 0.650 e 0.156 0.623 1.27 0.0121 0.0308 0.0069 e 0.0415

BDL 0.0144 BDL 0.0419 0.0444 0.105 BDL BDL 0.0036 BDL 0.0058

0.0089 0.150 0.040 1.09 3.12 4.41 0.0146 0.0165 0.0137 BDL 0.0447

0.0038 0.0468 e 0.270 0.704 1.03 0.0080 0.0065 0.0080 e 0.0225

0.0033 0.0578 e 0.460 1.35 1.89 0.0064 0.0068 0.0037 e 0.0142

SD: standard deviation. BDL: below detection level. DDTs: sum of DDE, DDD and DDT. HCHs: sum of a -, b-, g-, and d eHCH.

Table 2 Comparison between the present study and others studies on the surface soil of the Tibetan Plateau and farmland in the other regions (ng/g dw). Sampling sites

DDTs

HCHs

References

Tibetan agricultural soil Tibetan rape Tibetan highland barley Soil Tibetan remote soil Antarctica soil China Southern china Northern China Eastern China Central China India Southern United States North-western Spain Mexico South-western Spain Crops Tianjin, China(cabbage) Argentina(leek) Ghana (Lettuce) India(rice) Jiangsu, China(rice) Pakistan(rice) Pakistan(wheat) Turkey(wheat)

BDL-41.6 (1.36)a 0.105e4.41(1.03) 0.0071e7.77 (0.661)

BDL-8.36 (0.349) 0.0058e0.0447 (0.0225) BDL-0.229(0.0364)

This study This study This study

0.02e6.3 (0.882) 0.5e3.7

0.05e0.7(0.226) 0.49e1.34 0.2e23.9 (1.74) 4.4 3.6 2.41 15.4 825

Wang et al., 2012 Klanova et al., 2008 Niu et al., 2013 Gao et al., 2008 Tao et al., 2005 Jiang et al., 2009 Zhou et al., 2013 Mishra et al., 2012 Bidleman and Leone, 2004 Pereira et al., 2010 Waliszewski et al., 2008 Munoz-Arnanz and Jimenez, 2011

a

67.3 80.1 21.4 152 903 211 70.5 1.79 16 45.8 40 2-40 (23) BDL-53 (29) 2.72e36.6 (11.6) 0.55e15.2 (3.5) 0.9e310 (4.8)

200 3.5

38 17.7 130 13-113(66) BDL-39 (30) 1.48e27.6 (6.95) 0.35e4.53 (1.50) BDL-18.6 (2.2)

Tao et al., 2005 Gonzalez et al., 2003 Bempah et al., 2012 Babu et al., 2003 Chen et al., 2007 Mahmood et al., 2014 Mahmood et al., 2014 Guler et al., 2010

Value in bracket means the average value; BDL: below detection limit.

(200 ng/g dw for HCHs, Pereira et al., 2010), one magnitude lower than those in Mexico (70.5 and 3.5 ng/g dw for DDTs and HCHs, respectively, Waliszewski et al., 2008) and comparable to those in southwestern Spain (1.79 ng/g dw for DDTs, Munoz-Arnanz and Jimenez, 2011) (Table 2). In the TP, highland barley and rape are the main crops. In order to compare with other studies conveniently, all crop data are expressed on a dry weight basis. The arithmetical mean concentrations of DDTs and HCHs were 1.03 ± 1.89 and 0.0225 ± 0.0142 ng/ g dw in rape and 0.661 ± 1.27 and 0.0364 ± 0.0415 ng/g dw in barley (Table 1), respectively. The paired-samples T test shows that the concentrations of rape OCPs were not significantly different from those of the barley planted at the same sites (p > 0.05). The average concentration of DDTs and HCHs in the crop were lower than those in moss from Antarctic (4.21 and 2.30 ng/g dw respectively, Borghini et al., 2005) and comparable to those in the willows from the Arctic (0.13 and 0.821 ng/g dw respectively, Kelly and Gobas, 2001). Compared with the other vegetables from Tianjin, China (16 and 38 ng/g dw respectively, Tao et al., 2005), Argentina (45.8 and 17.7 ng/g dw Gonzalez et al., 2003) and Ghana (40 and 130 ng/g dw, respectively, Bempah et al., 2012), the concentrations of DDTs

and HCHs in rape were relatively lower (Table 2). Due to that highland barley is a rare species in other regions of the world, rice and wheat were chosen for comparison. The average concentrations of DDTs and HCHs in barley of the TP were nearly three orders of magnitude lower than those in rice from India (23 and 66 ng/g dw, respectively, Babu et al., 2003), Pakistan (11.6 and 6.95 ng/g dw, respectively, Mahmood et al., 2014) and China (29 and 30 ng/g dw, respectively, Chen et al., 2007) (Table 2). Compared to the wheat in the other countries, the levels of DDTs and HCHs in barley of the TP were also lower (Guler et al., 2010; Mahmood et al., 2014) (Table 2). In brief, compared with the other agricultural regions, the levels of DDTs and HCHs both in the agricultural soil and crops of the TP were relatively low in a global perspective. 3.2. Possible sources of DDTs and HCHs in the farmland The isomer ratios of DDTs are often used to evaluate whether the residues are from historical usage or fresh input. Generally, DDE and DDD are the degradation products of DDT (Boul, 1995). If the ratio of (DDE þ DDD)/DDT > 1, it indicates historical residues, while if the ratio < 1, it indicates fresh application (Munoz-Arnanz and

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Jimenez, 2011; Qiu et al., 2004). In the agricultural soil of the TP, more than 75% of the ratios for (DDE þ DDD)/DDT were higher than 1 (average value ¼ 2.72, Figure SI-1), which were similar with that in the Tibetan remote soil (average value ¼ 1.48, Wang et al., 2012). This phenomenon suggests that DDTs in the soil were mainly from historical residues. Different from the soil, the ratios of (DDE þ DDD)/DDT in barley and rape were all < 1 (Figure SI-1), which reflects that the DDTs in the crops may be from fresh application. This phenomenon obviously indicates that different DDT isomer ratios were obtained for the agricultural soil and crops, respectively, which is in line with the results of previous studies (Mikes et al., 2009; Trapp, 2015). Trapp (2015) hold the view that atmospheric deposition was the major uptake mechanism for the vegetation aerial tissues. Moreover, the statue of balance for DDTs and HCHs in the Tibetan farmland is deposition to the agricultural soil (Text SI-3, Table SI-6). Hence, the crops of this study probably absorbed the atmospheric DDTs. The average ratios of (DDE þ DDD)/DDT in the crops (0.229 for barley and 0.140 for rape) were similar with those in conifer needles (0.18) from the southeastern TP (Yang et al., 2008) and in pasture grass (0.14) from the central TP (Wang et al., 2015a). Therefore, the DDTs in the crops came from the same source as those in the other plants in the TP, namely atmospheric deposition. Additionally, the ratios of (DDE þ DDD)/DDT in the crops were also close to those of rice (0.17e0.65) from India (Babu et al., 2003). In our previous study, the Indian monsoon was found to be a driving force in pervading the atmospheric transport of DDTs from India to the TP (Sheng et al., 2013). The growing season of the crops coincides with the monsoon season (from May to September); therefore, the DDTs in the crops of this study likely originated from the on-going usage of parent DDT isomers in India (Zhang et al., 2008). The accumulation of DDTs in the crops only happened in the current year, whereas the soil DDTs were due to the perennial accumulation for many years. This may be the reason why the compositions of DDTs in crops are different from those in the soil. As pesticides, the HCHs include technical HCHs and Lindane that was used as a substitute after the ban of technical HCHs. The former is made up of a, b, g and d-HCH, and the latter is mainly g-HCH (accounting for approximately 99%) (Li et al., 2001; Zhang et al., 2011). In technical HCHs, the ratios of a/b-HCH and a/g-HCH were approximately 11.8 and 4.6e5.8, respectively (Niu et al., 2013; Zhang et al., 2011). The ratios of a/b-HCH in agricultural soil and crops are given in Figure SI-1. For both the agricultural soil and crops, the average ratios of a/b-HCH (soil: 0.591, barley: 1.18, rape: 0.817 Figure SI-1) were far lower than 11.8. b-HCH is the most stable HCH isomer (Willett et al., 1998). a-HCH and g-HCH were found to isomerize to b-HCH in the field environment (Wu et al., 1997). The relatively higher concentrations of b-HCH compared to a-HCH in agricultural soils/crops likely suggested that other HCH isomers have been transformed to b-HCH. Usually, this transformation takes years, and significant correlations were found between b-HCH and the total HCHs in the agricultural soils (R2 ¼ 0.93, p < 0.001 for soil, Figure SI-2). This good correlation suggested that the source of soil HCHs may be mainly from past residuals. The average ratios of a/g-HCH were 2.12, 1.18 and 1.08 in the Tibetan agricultural soil, barley and rape, respectively (Figure SI-1), which were all lower than 4.6. Compared with a-HCH, g-HCH has a higher water-solubility (Shen and Wania, 2005), and thus may experience greater wet deposition onto the soil and vegetation surface than a-HCH. This might be one possible reason that lower a/ g-HCH ratios were observed in soil of this study. Additionally, the average ratio of a/g-HCH in the crops (barley: 1.18, rape: 1.08, Figure SI-1) was similar with that in lichens from the southeastern TP (1.6, Yang et al., 2013), grazing grass from the eastern edge of the TP (1.3, Pan et al., 2014) and the central TP (1.8, Wang et al., 2015a).

The ratios of a/g-HCH in the crops were also close to those of rice (0.8e3.0) from India (Babu et al., 2003). Although technical HCHs were terminated, lindane (g-HCH) is still used as a pesticide in the agricultural area of India (Zhang et al., 2008). Similar to the DDT sources mentioned above, the parent HCH isomers (a,g-HCH) in the crops possibly also come from atmospheric deposition originating from India. Taking the results of all of the isomer ratios ((DDE þ DDD)/DDT, a/b-HCH and a/g-HCH) into consideration, the historical accumulation of OCPs in soil and the partitioning of fresh OCPs between the atmosphere and crop leaves could be concluded. Combined with the relatively lower OCP concentrations in soils and crops, the wide and extensive current usage of OCPs in the Tibetan agricultural region could be eliminated. For the OCPs in edible crops, their overall levels and chemical compositions are similar to those in other wild plants (such as pine needles and grazing grasses) in the plateau. This indicated that the OCPs in vegetation of the plateau may come from the same source, namely the fresh atmospheric input of OCPs from India. 3.3. Spatial distribution of DDTs and HCHs in agricultural soil and crops The spatial distribution of DDTs and HCHs in the agricultural soil and highland barley from different regions of the TP is depicted in Fig. 2. Due to the limited sample size (n ¼ 5), the spatial distribution of rape DDTs and HCHs will not be discussed in this study. The highest concentration of the DDTs in the agricultural soil appeared in the Nyingchi region (Fig. 2a, p,p0 -DDE is the dominant chemical). Nyingchi is adjacent to the Indian subcontinent and the Yarlung Tsangpo River valley is considered a “leaking wall” that contaminates the southeastern TP (Wang et al., 2015b). Higher concentrations of DDTs were also found in the remote soils collected from the Nyingchi region (Wang et al., 2012). The proximity of the Nyingchi region to the Indian subcontinent may lead to the high levels of DDTs in both remote soil and agricultural soil. However, the highest concentrations of HCHs in the Tibetan agricultural soil were found in the Qamdo region, far east of the TP (Fig. 2b, dominated by b-HCH). This is different from the previous study (Wang et al., 2012), in which the highest concentration of HCHs in remote Tibetan soil was found in southern Tibet. The difference in the HCH spatial distributions in agricultural soil and remote soil suggested that agricultural soil in the Qamdo region may be contaminated by more complicated HCH sources. Qamdo is located in a conjunction zone among the mainland of the Tibetan Plateau, the Sichuan province of China, and the Indian subcontinent. Sichuan is one of the major agricultural provinces of China. Due to its geographic position, Qamdo has a relatively long agricultural history compared to other regions of Tibet. This would be the reason that high amounts of HCH residues occurred in the agricultural soil of Qamdo. The highest and lowest concentrations of DDTs and HCHs in barley were found in the Nyingchi and Lhasa regions, respectively (Fig. 2c and d), and their concentrations declined from the east to west. This declining trend is broadly in agreement with the atmospheric distribution patterns of OCPs across the TP (Wang et al., 2010). 3.4. Human exposure risk assessment Although Arctic and Antarctic are remote regions, bioaccumulation of both legacy and emerging POPs in wildlife and human has been widely reported (Sladen et al., 1966; Zhu et al., 1995). High levels of these POPs have been found in biota of Polar regions and Inuit people (Gabrielsen, 2005; Goerke et al., 2004).

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Fig. 2. Spatial distribution of DDTs and HCHs in agricultural soil (a and b) and highland barley (c and d) from the Tibetan Plateau.

Additionally, the Inuit population received greater exposure risk of POPs than people anywhere else on the Earth (Donaldson et al., 2010; Hansen, 2000; Pacyna et al., 2015). Known as the “third pole”, the human exposure risk of Tibetan residence is of concern due to the combined contribution of LRAT and potential local contamination. According to the US EPA Exposure Factors Handbook (1997), the exposure risks to human are mainly through dietary and nondietary pathways. In the TP, food are consisted of crop, yak milk and meat, among which approximately 50% are crops (Liu et al., 2004). The exposure risks to humans via intake of crop were usually estimated based on the concentrations of soil OCPs and the bioaccumulation factors (BAFs) of chemicals (Niu et al., 2013). The BAFs were defined as [OCPs]crop/[OCPs]soil. In this study, the agricultural soil and crop samples were collected synchronously. Therefore, the valid BAFs for different crops in the TP were gained (Table SI-2). Considering the absence of inhalation toxicity factors for DDTs and HCHs, the non-carcinogenic risks by the inhalation pathway were excluded in this study. Based on the concentrations of soil OCPs and BAFs derived in this study, the non-carcinogenic risks of DDTs (p,p0 -DDE, o,p0 -DDT and p,p0 -DDT) and HCHs (a, b, g-HCH) via ingestion, dermal contact and the diet to children and adults were estimated (Table SI-7) and summarized in Table SI-8. The HI values are displayed in Fig. 3. The HI values of DDT and HCH isomers were all below 1 for both children and adults (Fig. 3), which represented that the noncarcinogenic risks of DDTs and HCHs are minor. Similar results were observed by previous studies on agricultural soil across China (Niu et al., 2013) and Hong Kong (Man et al., 2011). In addition, the

Fig. 3. Non-carcinogenic exposure risks to children and adults.

HI values of DDTs were higher than those of HCHs (Fig. 3), indicating that DDTs may pose a slightly larger non-carcinogenic risk than HCHs to humans. The non-carcinogenic risks of OCPs to adults were often higher than those to children (Fig. 3). The cancer risks due to exposure to DDTs and HCHs via ingestion, dermal contact, inhalation and diet to children and adults are

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summarized in Table SI-9. Most of the estimated cancer risks to children and adults due to exposure to p,p0 -DDE, o,p0 -DDT and HCHs (approximately 75%, Table SI-9) were lower than 106, indicating that the residents will be exposed to a very low cancer risks. Only a few sites showed cancer risks due to DDTs and HCHs of approximately 105 (Table SI-9). In these sites (2 located in the Nyingchi region, 2 located in the Qamdo region and 1 located in the Shannan region Table SI-10), consumption of agricultural food will induce low cancer risks. Similar with the non-carcinogenic risks, the cancer risks of DDTs and HCHs to the adults were both higher than those for children, which was probably due to the larger food intake by adults than children. In the assessment of non-carcinogenic and cancer risks of DDTs and HCHs, the exposure risks via the dietary pathway accounted for approximately 99% compared with the other pathways (Table SI-11). The same result was also discovered by a previous study (Niu et al., 2013). 4. Conclusion In the TP, the concentrations and composition of DDTs and HCHs in the agricultural soil and crops were similar with those in remote soil and wild plants, respectively. Both DDTs and HCHs in the agricultural soil were from historical residues, but the OCPs in the crops came from fresh input via atmospheric deposition. Generally, the DDTs and HCHs in the farmland will not pose non-carcinogenic and cancer risks to the local children and adults of the TP. However, highland barley and rape occupy only a part of the diet. The health risks due to exposure to DDTs and HCHs via dietary pathways in the TP need further research investigating other foods, such as meat, milk and eggs. Acknowledgments We would like to thank the staff at the Southeast Tibet Observation and Research Station for the Alpine Environment for helping with field sample collection. This study was supported by the National Natural Science Foundation of China (41222010 and 41071321) and the Youth Innovation Promotion Association (CAS2011067). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.chemosphere.2016.01.120. References Abhilash, P.C., Singh, N., 2009. Pesticide use and application: an Indian scenario. J. Hazard. Mater 165, 1e12. Agricultural geography of the Tibetan Plateau, 1984. Series Book of Tibet Science Expedition. Scientific Press, Beijing. Babu, G.S., Farooq, M., Ray, R.S., Joshi, P.C., Viswanathan, P.N., Hans, R.K., 2003. DDT and HCH residues in basmati rice (Oryza sativa) cultivated in Dehradun (India). Water Air. Soil Poll. 144, 149e157. Bempah, C.K., Buah-Kwofie, A., Enimil, E., Blewu, B., Agyei-Martey, G., 2012. Residues of organochlorine pesticides in vegetables marketed in Greater Accra Region of Ghana. Food control. 25, 537e542. Bidleman, T.F., Leone, A.D., 2004. Soil-air exchange of organochlorine pesticides in the Southern United States. Environ. Pollut. 128, 49e57. Borghini, F., Grimalt, J.O., Sanchez-Hernandez, J.C., Bargagli, R., 2005. Organochlorine pollutants in soils and mosses from Victoria Land (Antarctica). Chemosphere 58, 271e278. Chakraborty, P., Zhang, G., Li, J., Sivakumar, A., Jones, K.C., 2015. Occurrence and sources of selected organochlorine pesticides in the soil of seven major Indian cities: assessment of airesoil exchange. Environ. Pollut. 204, 74e80. Chen, S., Shi, L., Shan, Z., Hu, Q., 2007. Determination of organochlorine pesticide residues in rice and human and fish fat by simplified two-dimensional gas chromatography. Food Chem. 104, 1315e1319. Chung, S.W.C., Kwong, K.P., Yau, J.C.W., 2008. Dietary exposure to DDT of secondary school students in Hong Kong. Chemosphere 73, 65e69.

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