Dechlorane plus in greenhouse and conventional vegetables: Uptake, translocation, dissipation and human dietary exposure

Accepted Manuscript Dechlorane plus in greenhouse and conventional vegetables: Uptake, translocation, dissipation and human dietary exposure Jianqiang Sun, Yihua Wu, Ninger Tao, Li Lv, Xiaoyan Yu, Anping Zhang, Hong Qi PII:

S0269-7491(18)33592-9

DOI:

https://doi.org/10.1016/j.envpol.2018.10.094

Reference:

ENPO 11785

To appear in:

Environmental Pollution

Received Date: 4 August 2018 Revised Date:

17 October 2018

Accepted Date: 21 October 2018

Please cite this article as: Sun, J., Wu, Y., Tao, N., Lv, L., Yu, X., Zhang, A., Qi, H., Dechlorane plus in greenhouse and conventional vegetables: Uptake, translocation, dissipation and human dietary exposure, Environmental Pollution (2018), doi: https://doi.org/10.1016/j.envpol.2018.10.094. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT 1

SC

RI PT

Graphic Abstract

2

AC C

EP

TE D

M AN U

3

ACCEPTED MANUSCRIPT 1 2 3 4 5 6 7 8 9 10

RI PT

Dechlorane Plus in greenhouse and conventional vegetables: uptake, translocation, dissipation and human dietary exposure Jianqiang Sun a, Yihua Wu a, Ninger Tao a, Li Lv a, Xiaoyan Yu a, Anping Zhang a, *, Hong Qi b

11

14 15

a

International Joint Research Center for Persistent Toxic Substances, College of Environment, Zhejiang University of Technology, Hangzhou 310014, China b Department of Environmental Engineering, School of Municipal and Environmental Engineering, Harbin Institute of Technology, Harbin 150001, China

SC

12 13

AC C

EP

TE D

M AN U

16

*

To whom correspondence should be addressed. Phone: 86-571-8832-0534. Fax: 86-571-88871576. E-mail: [email protected] a Zhejiang University of Technology b Harbin Institute of Technology 1

ACCEPTED MANUSCRIPT

Abstract: In an attempt to evaluate the behavior of Dechlorane plus (DP) in soil-

18

vegetable systems, this work investigated the uptake and translocation of DP by

19

vegetables and the dissipation of DP in soil under greenhouse and conventional

20

conditions. To address human dietary exposure to DP, estimated dietary intake via

21

vegetable consumption was calculated. The uptake potential indexes of DP from soil

22

into root for tomato and cucumber cultivated under different conditions ranged from

23

0.089 to 0.71. The ranges of uptake potential indexes of DP from resuspended soil

24

particles into stem, leaf and fruit were 0.68-0.78, 0.27-0.42 and 0.39-0.75,

25

respectively. The uptake potential indexes in greenhouse vegetables were generally

26

higher than those in conventional vegetables when the vegetables had been planted in

27

contaminated soil, indicating that greenhouse enhanced the uptake of DP with a high

28

soil concentration by vegetables. The translocation factor (TF) values of DP in

29

vegetables were in the range of 0.022 to 0.17, indicating that DP can be transported

30

from root to fruit even though it has a high octanol water partition coefficient (KOW).

31

The half-lives of DP dissipation in soil ranged from 70 to 102 days. The dissipation of

32

DP in greenhouse soil was slightly slower than that in conventional soil. Higher

33

estimated dietary intake (EDI) values of DP via greenhouse vegetables were observed

34

due to the higher concentration of DP in greenhouse vegetables than conventional

35

vegetables. These results suggested that greenhouses should not be adopted for

36

vegetable production in contaminated regions.

37

Keywords: Greenhouse, Vegetables, Dechlorane plus, Estimated dietary intake

38

Capsule: Significant translocation was observed for compound with high

39

KOW and concentration in greenhouse vegetables.

AC C

EP

TE D

M AN U

SC

RI PT

17

40

2

ACCEPTED MANUSCRIPT 41 42

Introduction Dechlorane plus (DP) is a halogenated organic chemical that is widely used in electrical wire and cable coatings, plastic roofing materials, computer connectors and

44

other polymeric systems. It was developed as a substitute for Dechlorane (also called

45

Mirex), which had been used since the 1960s (Hoh et al., 2006). The annual

46

production of DP in the USA since 1986 is approximately 450-4500 tons, and that in

47

China since 2003 is 300-1000 tons (Qiu et al., 2007; Wang et al., 2010). It has been

48

estimated that 10 million pounds of DP are produced globally every year (Ren et al.,

49

2008). Although DP has been produced and used for more than 50 years, the first

50

environmental occurrence of DP was not reported until 2006, when it was found in the

51

Great Lakes in North America (Hoh et al., 2006). DP has been detected across the

52

world, including in Arctic regions and in the marine environment, because of its

53

chemical stability in various environmental media (Na et al., 2015; Moller et al., 2010;

54

Sverko et al., 2010; Sverko et al., 2008; Qi et al., 2010; Ma et al., 2014; Chen et al.,

55

2011; Wang et al., 2017) and long-range atmospheric transport potential (Moller et al.,

56

2011; Moller et al., 2012). The bioaccumulation and biomagnification of DP in the

57

freshwater food chain in e-waste recycling areas have been reported (Wu et al., 2010).

58

Recently, toxicological research has indicated that the oral exposure of mice to DP

59

can cause oxidative damage to the liver and perturbations to the metabolism and

60

signal transduction (Wu et al., 2012). DP has also been detected in the liver of

61

Sprague-Dawley rats and had an effect on the mRNA expression levels of some

62

enzymes and their activities (Li et al., 2013). Research based on protein responses has

63

suggested that DP may cause apoptosis in the liver of juvenile Chinese sturgeon

64

(Liang et al., 2014). These studies indicate that DP is a very harmful compound and

65

poses a potential threat to human health.

AC C

EP

TE D

M AN U

SC

RI PT

43

3

ACCEPTED MANUSCRIPT 66

The migration of halogenated organic pollutants from soil to vegetable has been considered to be the most important route of human exposure to such chemicals

68

(Navarro et al., 2017). The bioconcentration factors (BCFs) of halogenated organic

69

pollutants in vegetables are less than 1 in most cases (Zhang et al., 2015b),

70

demonstrating that the accumulation of organic pollutants by vegetation cannot reach

71

a significant extent (Simonich et al., 1995). However, organic pollutants can be

72

biomagnified to much higher levels through the food chain, thus presenting a high

73

exposure risk to the population (Kelly et al., 2007). The published studies that have

74

investigated the migration of halogenated organic pollutants from soil to vegetable

75

have mainly focused on chemicals including perfluorinated compounds,

76

polybrominated compounds and organochlorine pesticides (Clarke et al., 2011;

77

Lechner et al., 2011; Stahl et al., 2013; Felizeter et al., 2014; Huang et al., 2011;

78

Zhang et al., 2015a; Mariana et al., 2003). However, the data are currently insufficient

79

regarding the behavior of DP in the soil-vegetable system.

TE D

M AN U

SC

RI PT

67

In an attempt to fill this knowledge gap, the present work was designed to

81

investigate (i) the uptake of fresh and aged DP by greenhouse and conventional

82

vegetables, (ii) the translocation of fresh and aged DP within vegetables, (iii) the

83

dissipation of fresh and aged DP in greenhouse and conventional soil and (iv) the

84

estimated dietary ingestion of DP via vegetable consumption. The results were also

85

expected to address the concerns of human exposure to DP via vegetable consumption.

86

Experimental Sections

87

Chemicals

AC C

EP

80

88

Two DP isomers, i.e., syn-DP and anti-DP, were obtained from Wellington

89

Laboratories (Guelph, Canada). The fraction of anti-DP (fanti) is defined as the anti-DP

90

concentration divided by the total DP concentration (sum of syn- and anti-DP). 13C4

ACCEPTED MANUSCRIPT labeled surrogate standards, including decabrominated diphenyl ethers (13C12–BDE-

92

209), 2,2',3,4,5,5'-hexachlorobiphenyl (13C12–CB-141) and an internal standard of

93

2,2',3,3',5,5',6,6'-octachlorobiphenyl (13C12–CB-202), were purchased from

94

Cambridge Isotope Laboratories (Andover, MA, USA). Technical DP was obtained

95

from Anpon Electrochemical Company (Huaian, Jiangsu, China). Acetone,

96

dichloromethane and n-hexane (Tedia Company Inc, Shanghai, China) were of high-

97

performance liquid chromatography grade. The chemicals used for sample cleanup,

98

i.e., anhydrous sodium sulfate (Puhui Chemical Co., Ltd, Hangzhou, China), alumina,

99

silica gel and florisil (60-100 mesh, J&K Chemical, Shanghai, China) were heated at

100

180 °C for 12 h and baked at 450 °C for 4 h before use. The fiberglass filter (Yuyan

101

Co., Ltd, Shanghai, China) used to wrap the samples in the Soxhlet extraction was

102

baked overnight at 450 °C.

103

Field plot

SC

M AN U

The greenhouses used in this study were built with a bamboo frame and plastic

TE D

104

RI PT

91

film which were free of DP. The internal heat and light were exclusively dependent on

106

solar radiation. The greenhouse was equipped with no auxiliary heat or light sources.

107

These typical plastic greenhouses can only afford a suboptimal temperature and light

108

intensity for vegetable growth. The conventional vegetables were planted in an open

109

field in the period when the climatic conditions were the best suitable for vegetable

110

cultivation. The temperature, mean relative humidity and total solar radiation during

111

the growth period were 20 °C, 70% and 1170 MJ m-2, respectively, in the greenhouse

112

and 25 °C, 75% and 1450 MJ m-2, respectively, in the open conventional field. The

113

greenhouse vegetables had a longer growth period than did the conventional

114

vegetables in the present work. The greenhouse and conventional vegetables were

115

grown during the periods from January to June and from May to July, respectively, in

AC C

EP

105

5

ACCEPTED MANUSCRIPT 116

2014. The marketable date of the greenhouse vegetables

117

was one month ahead of that of the conventional vegetables. This difference in date

118

favored the greenhouse vegetables to merit higher prices than did the conventional

119

vegetables in a local market. The greenhouses were located on a farm in Zhejiang province, China (E

121

119°54′44″, N 30°5′28"). The open fields adjacent to the greenhouses were used to

122

plant conventional tomato and cucumber. All experiments were conducted at the farm. Twelve groups of samples, including tomato planted in background soil in the

SC

123

RI PT

120

greenhouse (TBG), tomato planted in background soil in the conventional open field

125

(TBC), cucumber planted in background soil in the greenhouse (CBG), cucumber

126

planted in background soil in the conventional open field (CBC), tomato planted in

127

soil containing fresh DP in the greenhouse (TFG), tomato planted in soil containing

128

fresh DP in the conventional open field (TFC), tomato planted in soil containing aged

129

DP in the greenhouse (TAG), tomato planted in soil containing aged DP in the

130

conventional open field (TAC), cucumber planted in soil containing fresh DP in the

131

greenhouse (CFG), cucumber planted in soil containing fresh DP in the conventional

132

open field (CFC), cucumber planted in soil containing aged DP in the greenhouse

133

(CAG) and cucumber planted in soil containing aged DP in the conventional field

134

(CAC), were used in this study. Each sample was prepared in triplicate.

136

TE D

EP

AC C

135

M AN U

124

The native soils at the farm were defined as background soils. The range of DP

concentrations in the farm soil was 3.3-3.5 ng g-1 dw.

137

To prepare the soils samples containing fresh DP, the background soil which

138

contained DP with concentration range of 3.3-3.5 ng g-1 dw were collected using a

139

hand-held coring device (Zhang et al., 2011) and then prepared by the following

140

procedure. Technical DP was dissolved in hexane to constitute a solution of 5000 mg 6

ACCEPTED MANUSCRIPT L-1. Volumes of 100, 200 300 and 400 mL were spiked into 5-kg masses of

142

background soil. Soil samples at each concentration level were prepared in

143

quadruplicate for the cultivation of greenhouse and conventional tomato and

144

cucumber. Following spiking, a subsample was collected in triplicate, wrapped in

145

cleaned aluminum foil, sealed in a plastic bag, and stored at -20 °C until analysis. The

146

rest of the spiked soil was placed back into the holes that had been dug in the

147

experimental area, and then tomato or cucumber was planted into the spiked soil.

To collect soil samples containing aged DP at different concentrations, four sites

SC

148

RI PT

141

around a DP manufacturing facility (Jiangsu Anpon Electrochemical Company,

150

Huai’an, China) were selected to sample soils. The collected soils were transferred to

151

the farm in Zhejiang. The soils from each site were separated into six fractions. Four

152

of these fractions were placed into the holes that had been dug in the greenhouse or

153

conventional field at the farm and were used to cultivate greenhouse tomato,

154

conventional tomato, greenhouse cucumber and conventional cucumber. The other

155

two fractions were placed into holes in the greenhouse and open field with the aim of

156

investigating the dissipation of DP in soil under greenhouse and conventional

157

conditions, respectively.

TE D

EP

To avoid interference between samples, all holes were separated by a distance of

AC C

158

M AN U

149

159

3 m. The spiked and collected soils that had been placed into the holes were covered

160

by a thin plastic film.

161

Sample collection

162

The whole plant was collected when the vegetables were marketable. After

163

harvest, the soil loosely adhering to the roots was removed by gently shaking and was

164

collected as samples. Then, the root, stem, leaves, and fruits of each plant were

7

ACCEPTED MANUSCRIPT 165

separated and then thoroughly washed with distilled water. Vegetables grown in each

166

soil were sampled in triplicate.

168 169

To investigate the dissipation of DP in soil, the samples were collected in triplicate on predetermined dates. All samples were stored at -20 °C until analysis. The water content of samples

RI PT

167

was determined by constant-weight drying in an oven at 60 °C. The concentration of

171

DP in samples was expressed on a dry-weight basis.

172

Extraction, cleanup, and analysis

173

SC

170

The detailed sample treatment procedure can be found in our previous study (Zhang et al., 2015a). Fresh soil samples of 10 g were thoroughly mixed with

175

anhydrous sodium sulfate. The tissue samples, that is, the roots, stems, leaves, and

176

fruits, were chopped into small pieces and then shredded to a paste by a pulper. The

177

5-g samples were thoroughly mixed with anhydrous sodium sulfate and Soxhlet-

178

extracted with 120 mL of dichloromethane for 24 h. The extracts were concentrated to

179

approximately 2 mL using a rotary evaporator and then purified in a silica, alumina

180

and florisil column. The effluent was eluted with 70 mL of a mixture of hexane and

181

dichloromethane (V/V, 7:3) and solvent-exchanged to n-hexane by rotary evaporation.

182

The samples were then blown down to exactly 1 mL by a gentle stream of high-purity

183

nitrogen and stored at -20 ºC before analysis.

TE D

EP

AC C

184

M AN U

174

The DP concentrations were analyzed by an Agilent 7890A gas chromatograph

185

coupled with an Agilent 5975C mass spectrometer (GC-MS) equipped with a DB-

186

5MS capillary column (15 m×0.25 mm i.d., 0.10 µm film thickness) using electron

187

capture negative ionization (ECNI) in full-scan and selected ion monitoring modes

188

(Agilent Technologies Inc. (China), Beijing, China). The temperature program was

189

initiated at 90 °C, held for 1 min, increased to 180 °C at 20 °C min-1 for 2 min, 8

ACCEPTED MANUSCRIPT increased to 330 °C at 8 °C min-1, and finally held for 5 min. Helium (purity

191

≥99.999%) and methane (purity ≥99.999%) were used as the carrier gas at a flow rate

192

of 1.0 mL min-1 and as the chemical ionization moderating gas, respectively. The

193

temperature of the injection port, transfer line, ion source and quadrupole was 280,

194

290, 200 and 150 °C, respectively. The molecular ions fragments m/z 653.8 and 651.8

195

were monitored for syn-DP and anti-DP.

196

Quality assurance and quality control (QA/QC)

Anhydrous sodium sulfate that had been exposed in the greenhouse and

SC

197

RI PT

190

conventional field for 1 min were used as field blanks. They were treated the same as

199

the samples throughout the procedure. The surrogate standards (including 13C12–BDE-

200

209 and 13C12–CB-141) were added to all samples before extraction. The recoveries of

201

the surrogates were in the range of 60%-110%. The DP concentration in samples was

202

not corrected by the surrogate recoveries (Qiu et al., 2007; Ren et al., 2008; Qi et al.,

203

2010). Spike recovery experiments were conducted by spiking DP into samples that

204

had been collected from background sites and subsequently analyzing the spiked

205

samples in the same manner as that used for the standard samples. The recovery was

206

calculated as the difference between the detectable amount and native amount in the

207

spiked sample divided by the spiked amount. The mean recoveries were 91±7% for

208

syn-DP and 94±9% for anti-DP in the soil, 85±17% for syn-DP and 89±22% for anti-

209

DP in the root, 82±21% for syn-DP and 85±22% for anti-DP in the stem, 78±19% for

210

syn-DP and 82±20% for anti-DP in the leaf, and 78±10% for syn-DP and 80±20% for

211

anti-DP in the fruit. The method detection limit (MDL) was defined as the ratio

212

between the amount of DP that had a chromatographic peak with a signal/noise ratio

213

of 10 and the dry weight of the sample. The calculated MDLs of syn-DP and anti-DP

214

were 2.2 and 3.1 pg g-1 dw for the soil, 4.1 and 4.7 pg g-1 dw for the root, 13 and 14

AC C

EP

TE D

M AN U

198

9

ACCEPTED MANUSCRIPT pg g-1 dw for the stem, and 102 and 114 pg g-1 dw for the fruit. 13C-labeled

216

2,2',3,3',5,5',6,6'-octa chlorobiphenyl (13C12–CB-202) was added to the samples as an

217

internal standard before injection. Procedural blanks were run with every set of 10

218

samples throughout the study. No DP was found in the blanks. Each sample was

219

analyzed in triplicate.

220

Statistical Analysis

RI PT

215

All statistical analysis was performed in Origin for Windows (Version 8.0,

222

OriginLab (Guangzhou) Ltd, Guangzhou, China). The t-test was used to confirm the

223

significant difference between two samples. The difference was considered to be

224

significant when the p-value was less than 0.05.

225

Results and discussion

226

Uptake of DP from soil into vegetable roots

M AN U

227

SC

221

The DP concentrations and the fanti in soils and vegetable tissues under different conditions are shown in Table 1 and Table 2 as arithmetic means and standard

229

deviations, respectively. The fanti values in all samples were not significantly different

230

from that (0.700±0.009) in technical DP (Wu et al., 2010) (Table 2), implying that

231

isomer-specific degradation and transportation of DP did not occur in the soil-

232

vegetable system. Statistical analysis indicated that the DP concentrations in

233

background soils and vegetables planted in background soils were not significantly

234

different between greenhouse samples and conventional samples. This result was

235

similar to that in a previous study that indicated that the organochlorine pesticide

236

(OCP) content in soil and vegetables was not significantly different between

237

greenhouse and conventional conditions (Zhang et al., 2015a). Both the native DP and

238

OCP concentrations in the background soils had relatively low levels of less than 10

239

ng g-1. For the vegetables planted in contaminated soils containing a high

AC C

EP

TE D

228

10

ACCEPTED MANUSCRIPT concentration of fresh or aged DP (Table 1), the DP concentrations in the greenhouse

241

vegetables were significantly higher than those in the conventional vegetables. This

242

might be caused by the longer growth period of the vegetables in the greenhouse than

243

that of the vegetables in the open field. This implied that greenhouse cultivation did

244

produce a profound effect on the uptake of high soil concentrations of pollutants by

245

vegetables compared with conventional cultivation. On the basis of the results, it is

246

argued that greenhouses should be not allowed to produce vegetables at sites where

247

the soil is contaminated by high concentrations of pollutants, such as sites around e-

248

waste recycling and manufacturing facilities.

SC

RI PT

240

Bioaccumulation factors (BAFs) which were calculated as the concentration

250

ratios between tissue and environmental matrix were usually used as uptake potential

251

indexes to evaluate the uptake potential of organic compounds from the soil into

252

plants. The calculation of BAFs was generally based on the assumption that the

253

concentrations of pollutants in soil to keep relatively constant (Tao et al., 2005; Zhang

254

et al., 2015a). However, the DP concentration in soil varied very much during

255

planting period in this work (Table 1). Therefore, the BAFs were not the best choice

256

to evaluate the uptake potential of organic compounds from the soil into plants in the

257

work. A significant concentration decrease of DP in soils was observed during

258

vegetable cultivation in the work (Table 1). The loss was induced by wash out,

259

volatilization, degradation and plant uptake. Thus, it can be deduced that a proportion

260

of DP loss in the soil was absorbed by roots. The index, DP concentration in the root

261

divided by the loss of DP concentration in the soil (RSLCRs), can indicate how much

262

DP was adsorbed by plant root from soil among total DP losses in soil. According to

263

the definition, RSLCRs can also be used as uptake potential indexes to evaluate the

264

uptake potential of pollutants from soils by plant. As shown in Table 3, the RSLCRs

AC C

EP

TE D

M AN U

249

11

ACCEPTED MANUSCRIPT of tomato and cucumber cultivated under different conditions ranged from 0.089 to

266

0.71. To the best of our knowledge, there are only two studies that investigated the

267

uptake potential of DP from soils by rice, spinach and tomato using root

268

bioaccumulation factors (RBAFs) before this work (Zhang et al., 2015b). The authors

269

reported RBAFs in the range of 0.32 to 2.2 for rice, 9.5 to 40 for spinach, and 1.6 to

270

7.7 for tomato, which were generally higher than RSLCRs values found in this work.

271

It was noted in the previous studies that the rice was sampled during the immature

272

period and the spinach and tomato were planted in biosolids-amended soils (Navarro

273

et al., 2017; Zhang et al., 2015b). The growth dilution might explain the higher uptake

274

potential of DP for young rice than for mature tomato (Zhang et al., 2015a). The

275

organic waste might have enhanced the uptake of DP by vegetables grown in

276

biosolids-amended soils and therefore resulted in the higher BAFs for the spinach and

277

tomato in the previous work than that for the tomato in this study. Additionally, the

278

difference in plant species and environmental conditions might also have contributed

279

to the differences in uptake potential of DP by plant among these studies (Simonich et

280

al., 1995).

SC

M AN U

TE D

The arithmetic means of RSLCRs in greenhouse vegetables were higher than

EP

281

RI PT

265

those in conventional vegetables in most cases. The difference in RSLCRs between

283

greenhouse and conventional vegetables might be produced by the greater adsorption

284

of pollutants by greenhouse vegetables than by conventional vegetables, due to the

285

longer growth period of the former (Zhang et al., 2015a). A further study investigating

286

RSLCRs indicated that vegetables planted in soil containing fresh DP had higher

287

RSLCRs than vegetables planted in soil containing aged DP. This might be caused by

288

the higher bioaccessibility of fresh DP than aged DP (Scelza et al., 2010).

289

Uptake of DP from resuspended soil particles into aerial parts of vegetables

AC C

282

12

ACCEPTED MANUSCRIPT 290

In addition to the root, the aerial parts of vegetation can also accumulate organic pollutants via the following three pathways (Wu et al., 2010; Zhang et al., 2015b;

292

Simonich et al., 1995; Kerstin et al., 1995): (i) partitioning from contaminated soil to

293

the roots and then translocation in the plant by the xylem, (ii) volatilization from soil

294

and then gas-phase deposition onto aerial parts, and (iii) subsequent deposition of

295

resuspended soil particles on aerial parts. For compounds with a high KOA and a low

296

concentration at the background level, the former two pathways cannot contribute

297

appreciable accumulation to the aerial parts of vegetation (Trapp et al., 2007; Ren et

298

al., 2008; Mikes et al., 2009; Huang et al., 2011; Huang et al., 2010). Instead, the third

299

pathway has been suggested to be a dominant contributor to organic pollutant

300

accumulation in the aerial parts of vegetation (Mikes et al., 2009). In the present work,

301

vegetables that had been planted in background soil were used to evaluate the uptake

302

of DP from resuspended soil particles into the aerial parts of vegetables. The stem

303

BAFs (SBAFs), leaf BAFs (LBAFs) and fruit BAFs (FBAFs) were calculated as stem,

304

leaf and fruit concentrations divided by background resuspended soil particles

305

concentrations, respectively (Zhang et al., 2015a; Simonich et al., 1995; Trapp et al.,

306

2007). The results are shown in Table 4. The average SBAFs, LBAFs and FBAFs of

307

greenhouse vegetables were slightly higher than those of conventional vegetables, but

308

there was no significant difference. Compared with conventional vegetables,

309

greenhouse vegetables had a longer growth period and received less rainfall, wind and

310

sun. These factors might contribute to the slightly higher BAFs of greenhouse

311

vegetables because the lower rainfall, wind and sun in the greenhouse were favorable

312

to increased soil-particle-phase DP deposition in the aerial parts of greenhouse

313

vegetables (Zhang et al., 2015a).

314

Translocation of DP in vegetables

AC C

EP

TE D

M AN U

SC

RI PT

291

13

ACCEPTED MANUSCRIPT 315

The translocation potential of DP from the vegetable root to fruit was evaluated by the translocation factor, which was calculated by the following equation.

317

TF = (Cfruit s- Cfruit b)/Croot s

318

where TF is the translocation factor; Cfruit s is the DP concentration in the fruit of

319

vegetables planted in soil spiked with fresh DP or polluted with aged DP; Cfruit b is the

320

DP concentration in the fruit of vegetables planted in background soil; and Croot s is

321

the DP concentration in the root of vegetables planted in soil spiked with fresh DP or

322

polluted with aged DP. The difference between Cfruit s and Cfruit b is that DP in fruit

323

from foliar uptake is eliminated and can only be contributed by translocation.

SC

The TF values under different conditions were in the range of 0.022 to 0.17, and

M AN U

324

RI PT

316

the detailed values are shown in Table 5. Similar results were also observed for the

326

accumulation of DP in 14 types of vegetables planted at an e-waste recycling site

327

(Wang et al., 2016) and in spinach and the aerial parts of tomato grown in biosolids-

328

amended soils (Navarro et al., 2017), the accumulation of legacy OCPs in aerial parts

329

of vegetables in a field (Zhang et al., 2015a; Gonzalez et al., 2003; Gonzalez et al.,

330

2005; Tao et al., 2005; Hulster et al., 1993; Wu et al., 2013), and the accumulation of

331

polyhalogenated compounds (PHCs) in rice (Zhang et al., 2015b). All these

332

observations indicated that compounds with a high KOW can enter the plant and that a

333

significant amount of these compounds can be transported from root to fruit if their

334

concentrations in soil are high enough. Thus, more attention should be paid to the

335

safety of vegetables from regions that are adjacent to waste-processing facilities and

336

toxic-compound manufacturing and use facilities.

AC C

EP

TE D

325

337

In the present work, the TF values in greenhouse vegetables were higher than

338

those in conventional vegetables, and the TF values for fresh DP were higher than

339

those for aged DP. This might be caused by the longer growth period of greenhouse 14

ACCEPTED MANUSCRIPT 340

vegetables than of conventional vegetables and the higher bioaccessibility of fresh DP

341

than aged DP (Zhang et al., 2015a; Scelza et al., 2010).

342

Dissipation of DP in greenhouse and conventional surface soils

343

The dissipation of chemicals in greenhouse and conventional soil could be fitted by first-order kinetics reasonably well (Wu et al., 2013). The half-lives of DP

345

dissipation under different conditions are shown in Fig. 1. The dissipation rates of DP

346

were in good agreement with those in spiked and contaminated soil during the

347

vegetable growth period in this study (Table 1) and a previous study (Zhang et al.,

348

2015b). The DP concentrations in background soil before planting were not

349

significantly different from those after planting. This might be caused by the input of

350

DP compensated the loss of DP in the soil during the planting period at the

351

experimental site. However, this input is negligible compared with the DP in spiked

352

and contaminated soil, because it did not produce an apparent effect on the dissipation

353

of DP in the two soils.

TE D

M AN U

SC

RI PT

344

The half-lives of DP dissipation in greenhouse soil were longer than those in

355

conventional soil. Similar results have also been observed in the dissipation of the

356

plant growth retardants paclobutrazol and uniconazole in greenhouse and

357

conventional soil: the dissipation of both chemicals was much slower in greenhouse

358

soil than conventional soil (Wu et al., 2013). It was noted that the conventional soil

359

received much more rainfall than the greenhouse at the experimental site. Leaching,

360

which is caused by rainfall, has been demonstrated to be an important contributor to

361

the difference in dissipation between greenhouses and open fields (Wu et al., 2013).

362

The present work was conducted at the same site as the previous study. Thus, it can be

363

reasonably assumed that the faster dissipation of DP in conventional soil than

364

greenhouse soil might also be influenced by the difference in rainfall. Further

AC C

EP

354

15

ACCEPTED MANUSCRIPT investigation into the effect of greenhouse use on the dissipation of DP and plant

366

growth retardants has indicated that greenhouse use had a more potent effect on plant

367

growth retardants than on DP; that is, the difference in plant growth retardant

368

dissipation between the greenhouse and conventional soil was greater than the

369

difference in DP dissipation. This might be caused by the higher solubility and lower

370

KOW of plant growth retardants than DP, because chemicals with a higher solubility

371

and lower KOW are more easily washed away by rainfall (Wu et al., 2013). Thus, it

372

was concluded that solubility and KOW play important roles in the difference in

373

dissipation of chemicals between the greenhouse and open field.

SC

The half-lives of fresh DP were slightly less than those of aged DP, implying that

M AN U

374

RI PT

365

375

the fresh DP dissipated faster than the aged DP. In contrast to aged DP, fresh DP

376

might be less strongly bonded with soil and thus was more easily accessed and

377

degraded by microbes in soil (Scelza et al., 2010).

This work focused on DP, but there are several other Dechlorane analogues, such

TE D

378

as Dechlorane 602 (Dec 602), Dechlorane 603 (Dec 603) and Dechlorane 604 (Dec

380

604), that had been discovered relatively recently as environmental contaminants

381

(Shen et al., 2011; Sun et al., 2013; Ren et al., 2008). The logKow values of Dec 602,

382

Dec 603, Dec 604 and DP were 8.1, 11.2, 11.3 and 11.3, respectively (Shen et al.,

383

2011). It can be deduced that Dec 603 and Dec 604 have similar environmental

384

behaviors in the interface between soil and plant with DP, because they have similar

385

Kow value. Dec 602 was easily absorbed by plants because of relatively small Kow

386

values (Qiu et al., 2008; Shen et al., 2010).

387

Estimation of daily DP intake via tomato and cucumber consumption

388 389

AC C

EP

379

The dietary DP intake via cucumber and tomato consumption was calculated by the following equation: 16

ACCEPTED MANUSCRIPT 390 391

EDI = C×FCR where EDI is the estimated daily intake (ng d −1); C is the concentration of DP in cucumber and tomato samples (ng g −1 wet weight); and FCR is the average tomato

393

and cucumber consumption per person per day (g d −1). The FCR values in the present

394

study were calculated by the consumption rates published in a previous study (Huo et

395

al., 2015). The average FCR values were approximately 78 g d −1 and 87 g d −1 for

396

tomato and cucumber in China, respectively.

The EDIs of DP via tomato and cucumber consumption under different

SC

397

RI PT

392

conditions are presented in Table 6. Greenhouse vegetable consumption resulted in

399

higher EDIs than did conventional vegetable consumption, suggesting that the

400

adoption of greenhouses in vegetable production would amplify the human exposure

401

risk to DP via vegetable consumption.

402

M AN U

398

The EDI of DP via background vegetable consumption was significantly higher than those of seafood (0.02-0.89 ng d −1) from the Xuande Atoll, South China Sea

404

(Sun et al., 2017), but was much lower than those of home-produced eggs (32-5038

405

ng d −1) from an e-waste recycling site, southern China (Zeng et al., 2016; Zheng et al.,

406

2012). The total EDIs of DP via all food consumption by an average Japanese and

407

Korean resident were estimated to be 576 pg d-1 and 11 ng d-1, respectively (Kakimoto

408

et al., 2014; Kim et al., 2014; ). These values were lower than that of a Chinese

409

resident via background vegetable consumption. These results indicated that DP

410

exposure via vegetable consumption is a potential health concern in China, especially

411

in regions heavily contaminated by DP.

412

AC C

EP

TE D

403

In summary, the present study showed that greenhouse can significantly enhance

413

the uptake of DP of high concentration by vegetables. This resulted in a higher

414

concentration of DP in greenhouse vegetables than in conventional vegetables. Thus, 17

ACCEPTED MANUSCRIPT it is not surprising that high EDI values of DP via greenhouse vegetable consumption

416

were observed. The results suggested a topic of concern that the pollutions of

417

vegetables planted on contaminated sites can be increased by adoption of greenhouses

418

and that the potential adverse effects of DP in greenhouse vegetables on human health

419

should be further investigated.

RI PT

415

420 421

Acknowledgments

This study was supported by the Natural Science Foundation of Zhejiang

423

Province (LY17B070006), the National Natural Science Foundation of China

424

(21577127, 21307111), the College Student Science and Technology Innovation

425

Program of Zhejiang Province (Xinmiao Talents Program) and the State Key

426

Laboratory of Urban Water Resource and Environment, Harbin Institute of

427

Technology (No. QAK201715).

429

TE D

428

M AN U

SC

422

References

431

Chen, S. J., Tian, M., Wang, J., Shi, T., Luo, Y., Luo, X, J., Mai, B, X., 2011.

432

Dechlorane plus (DP) in air and plants at an electronic waste (e-waste) site in south

433

China. Environ. Pollut. 159, 1290-1296.

434

Clarke, B. O., Smith, S. R., 2011. Review of ‘emerging’ organic contaminants in

435

biosolids and assessment of international research priorities for the agricultural use of

436

biosolids. Environ. Int. 37, 226-247.

437

Felizeter, S., McLachlan, M. S., De Voogt, P., 2014. Root uptake and translocation of

438

perfluorinated alkyl acids by three hydroponically grown crops. J. Agric. Food Chem.

AC C

EP

430

18

ACCEPTED MANUSCRIPT 62, 3334-3342.

440

Gonzalez, M., Miglioranza, K. S. B., Moreno, J. E. A. D., Moreno, V. J., 2005.

441

Evaluation of conventionally and organically produced vegetables for high lipophilic

442

organochlorine pesticide (OCP) residues. Food Chem. Toxicol. 43, 261-269.

443

Gonzalez, M., Miglioranza, K. S. B., Moreno, J. E. A. D., Moreno, V. J., 2003.

444

Occurrence and distribution of organochlorine pesticides (OCPs) in tomato

445

(Lycopersicon esculentum) crops from organic production. J. Agric. Food Chem. 51,

446

1353-1359.

447

Hoh, E., Zhu, L., Hites, R., 2006. A. Dechlorane plus, a chlorinated flame retardant, in

448

the great lakes. Environ. Sci. Technol. 40, 1184-1189.

449

Huang, H. L., Zhang, S. Z., Christie, P., 2011. Plant uptake and dissipation of PBDEs

450

in the soils of electronic waste recycling sites. Environ. Pollut. 159, 238-243.

451

Huang, H. L., Zhang, S. Z., Christie, P., Wang, S., Xie, M., 2010. Behavior of

452

decabromodiphenyl ether (BDE-209) in the soil plant system: Uptake, translocation,

453

and metabolism in plants and dissipation in soil. Environ. Sci. Technol. 44, 663-670.

454

Huo, L. P., 2015. Forecast on China's main fruit and vegetable consumption.

455

Agricultural Outlook. 11, 75-81.

456

Hulster, A., Matschner, H., 1993. Transfer of PCDD/PCDF from contaminated soils

457

to food and fodder crop plants. Chemosphere. 27, 439-446.

458

Kakimoto, K., Nagayoshi, H., Takagi, S., Akutsu, K., Konishi, Y., Kajimura, K.,

459

Hayakawa, K., Toriba, A., 2014. Inhalation and dietary exposure to dechlorane plus

460

and polybrominated diphenyl ethers in Osaka, Japan. Ecotox. Environ. Safe. 99, 69-

461

73.

AC C

EP

TE D

M AN U

SC

RI PT

439

19

ACCEPTED MANUSCRIPT Kelly, B. C., Ikonomou, M. G., Blair, J. D., Morin, A. E., Gobas, F. A. P. C., 2007.

463

Food web–specific biomagnification of persistent organic pollutants. Science 317,

464

236-239.

465

Kerstin, W. P., Michael, S. M., Gunther, U., 1995. Determination of the principal

466

pathways of poluchorinated debenzo-p-dioxins and dibenzofurans to lolium

467

multiflorum (welsh ray grass). Environ. Sci. Technol. 29, 1090-1098.

468

Kim, J., Son, M. H., Kim, J., Suh, J., Kang, Y., Chang, Y. S., 2014. Assessment of

469

dechlorane compounds in foodstuffs obtained from retail markets and estimates of

470

dietary intake in Korean population. J. Hazard. Mater. 275, 19-25.

471

Lechner, M., Knapp, H., 2011. Carryover of perfluorooctanoic acid (PFOA) and

472

perfluorooctane sulfonate (PFOS) from soil to plant and distribution to the different

473

plant compartments studied in cultures of carrots (Daucus carota ssp. Sativus),

474

potatoes (Solanum tuberosum), and cucumbers (Cucumis sativus). J. Agric. Food

475

Chem. 59, 11011-11018.

476

Li, Y., Yu, L. H., Wang, J. S., Wu, J. P., Mai, B. X., Dai, J. Y., 2013. Accumulation

477

pattern of dechlorane plus and associated biological effects on rats after 90 d of

478

exposure. Chemosphere. 90, 2149-2156.

479

Liang, X. F., Li, W., Martyniuk, C. J., Zha, J. M., Wang, Z. J., Cheng, G., Giesy, J. P.,

480

2014. Effects of dechlorane plus on the hepatic proteome of juvenile Chinese sturgeon

481

(Acipenser sinensis). Aquat. Toxicol. 148, 83-91.

482

Ma, J., Qiu, X. H., Liu, D., Zhao, Y. F., Yang, Q. Y., Fang, D., 2014. Dechlorane plus

483

in surface soil of north china: Levels, isomer profiles, and spatial distribution. Environ.

484

Sci. Pollut. R. 21, 8870-8877.

AC C

EP

TE D

M AN U

SC

RI PT

462

20

ACCEPTED MANUSCRIPT Mariana, G., Karina, S. B. M., Julia, E. A. D. M., Victor, J. M., 2003. Occurrence and

486

distribution of organochlorine pesticides (OCPs) in tomato (Lycopersicon esculentum)

487

crops from organic production. J. Agric. Food Chem. 51, 1353-1359.

488

Möller, A., Xie, Z. Y., Caba, A., Sturm, R., Ebinghaus, R., 2012. Occurrence and air-

489

seawater exchange of brominated flame retardants and dechlorane plus in the north

490

sea. Atmos. Environ. 46, 346-353.

491

Möller, A., Xie, Z. Y., Cai, M. H., Zhong, G. C., Huang, P., Cai, M. G., Sturm,

492

R., He, J. F., Ebinghaus, R., 2011. Polybrominated diphenyl ethers vs alternate

493

brominated flame retardants and dechloranes from east asia to the arctic. Environ. Sci.

494

Technol. 45, 6793-6799.

495

Möller, A., Xie, Z. Y., Sturm, R., Ebinghaus, R., 2010. Large-scale distribution of

496

dechlorane plus in air and seawater from the arctic to Antarctica. Environ. Sci.

497

Technol. 44, 8977-8982.

498

Mikes, O., Cupr, P., Trapp, S., Klanova, J., 2009. Uptake of polychlorinated biphenyls

499

and organochlorine pesticides from soil and air into radishes (Raphanussativus).

500

Environ. Pollut. 15, 488-496.

501

Na, G., Wei, W., Zhou, S. Y., Gao, H., Ma, X. D., Qiu, L. N., Ge, L. K., Bao, C. G.,

502

Yao, Z. W., 2015. Distribution characteristics and indicator significance of

503

dechloranes in multi-matrices at ny-Ålesund in the arctic. J. Environ. Sci.-China. 28,

504

8-13.

505

Navarro, I., de la Torre, A., Sanz, P., Porcel, M. A., Pro, J., Carbonell, G., Martinez,

506

M. D., 2017. Uptake of perfluoroalkyl substances and halogenated flame retardants by

507

crop plants grown in biosolids-amended soils. Environ. Res. 152, 199-206.

508

Qiu, X., Marvin, C. H., Hites, R. A., 2007. Dechlorane plus and other flame retardants

509

in a sediment core from lake ontario. Environ. Sci. Technol. 41, 6014-6019.

AC C

EP

TE D

M AN U

SC

RI PT

485

21

ACCEPTED MANUSCRIPT Qiu, X. H., Hites, R. A., 2008. Dechlorane plus and other flame retardants in tree bark

511

from the northeastern United States. Environ. Sci. Technol. 42, 31-36.

512

Qiu, X. H., Marvin, C. H., Hites, R. A., 2007. Dechlorane plus and other flame

513

retardants in a sediment core from lake ontario. Environ. Sci. Technol. 41, 6014-6019.

514

Qi, H., Liu, L. Y., Jia, H. L., Li, Y. F., Ren, N. Q., You, H., Shi, X. Y., Fan, L. L.,

515

Ding, Y. S., 2010. Dechlorane plus in surficial water and sediment in a northeastern

516

Chinese river. Environ. Sci. Technol. 44, 2305-2308.

517

Ren, N., Sverko, E., Li, Y. F., Zhang, Z., Harner, T., Wang, D., Wan, X., McCarry, B.

518

E., 2008. Levels and isomer profiles of dechlorane plus in Chinese air. Environ. Sci.

519

Technol. 42, 6476-6480.

520

Scelza, R., Rao, M. A., Gianfreda, L., 2010. Properties of an aged phenanthrene-

521

contaminated soil and its response to bioremediation processes. J. Soil Sediment. 10,

522

545-555

523

Shen, L., Reiner, E. J., Helm, P. A., Marvin, C. H., Hill, B., Zhang, X., Macpherson,

524

K. A., Kolic, T. M., Tomy, G. T., Brindle, I. D., 2011. Historic Trends of dechloranes

525

602, 603, 604, dechlorane plus and other norbornene derivatives and their

526

bioaccumulation potential in lake ontario. Environ. Sci. Technol. 45, 3333-3340.

527

Shen, L., Reiner, E. J., Macpherson, K. A., Kolic, T. M., Sverko, E., Helm, P. A.,

528

Bhavsar, S. P., Brindle, I. D., Marvin, C.H., 2010. Identification and screening

529

analysis of halogenated norbornene flame retardants in the laurentian great lakes:

530

Dechloranes 602, 603, and 604. Environ. Sci. Technol. 44, 760-766.

531

Simonich, S. L., Hites, R. A., 1995. Organic pollutant accumulation in vegetation.

532

Environ. Sci. Technol. 29, 2905-2914.

533

Stahl, T., Riebe, R. A., Falk, S., Failing, K., Brunn, H., 2013. Long-term lysimeter

534

experiment to investigate the leaching of perfluoroalkyl substances (PFASs) and the

AC C

EP

TE D

M AN U

SC

RI PT

510

22

ACCEPTED MANUSCRIPT carry-over from soil to plants: Results of a pilot study. J. Agric. Food Chem. 61,

536

1784-1793.

537

Sun, Y. X., Hu, Y. X., Zhang, Z. W., Xu, X. R., Li, H. X., Zuo, L. Z., Zhong, Y., Sun,

538

H., Mai, B. X., 2017. Halogenated organic pollutants in marine biota from the xuande

539

atoll, south China sea: Levels, biomagnification and dietary exposure. Mar. Pollut.

540

Bull. 118, 413-419.

541

Sverko, E., Reiner, E. J., Tomy, G. T., Tomy, G. T., McCrindle, R., Shen, L.,

542

Arsenault, G., Zaruk, D., MacPherson, K. A., Marvin, C. H., Helm, P. A., McCarry,

543

B. E., 2010. Compounds structurally related to dechlorane plus in sediment and biota

544

from lake ontario (Canada). Environ. Sci. Technol. 44, 574-579.

545

Sverko, E., Tomy, G. T., Marvin, C. H., Mccarry B. E., 2008. Dechlorane plus levels

546

in sediment of the lower great lakes. Environ. Sci. Technol. 42, 361-366.

547

Tao, S., Xu, F. L., Wang, X. J., Liu, W. X., Gong, Z. M., Fang, J. Y., Luo, Y. M.,

548

2005. Organochlorine pesticides in agricultural soil and vegetables from tianjin,

549

China. Environ. Sci. Technol. 39, 2494-2499.

550

Trapp, S., 2007. Fruit tree model for uptake of organic compounds from soil and air.

551

Sar Qsar Environ. Res. 18, 367-387.

552

Wang, D. G., Yang, M., Qi, H., Sverko, E., Ma, W. L., Li, Y. F., Alaee, M., Reiner, E.

553

J., Shen, L., 2010. An asia-specific source of dechlorane plus: Concentration, isomer

554

profiles, and other related compounds. Environ. Sci. Technol. 44, 6608-6613.

555

Wang, G. G., Peng, J. L., Hao, T., Feng, L. J., Liu, Q. L., Li, X. G., 2017. Effects of

556

terrestrial and marine organic matters on deposition of dechlorane plus (DP) in marine

557

sediments from the southern yellow sea, China: Evidence from multiple biomarkers.

558

Environ. Pollut. 230, 153-162.

AC C

EP

TE D

M AN U

SC

RI PT

535

23

ACCEPTED MANUSCRIPT Wang, S. R., Wang, Y., Luo, C. L., Li, J., Yin, H., Zhang, G., 2016. Plant selective

560

uptake of halogenated flame retardants at an e-waste recycling site in southern China.

561

Environ. Pollut. 214, 705-712.

562

Wu, J. P., Zhang, Y., Luo, X. J., Wang, J., Chen, S. J., Guan, Y.-T., Mai, B. X., 2010.

563

Isomer-specific bioaccumulation and trophic transfer of dechlorane plus in the

564

freshwater food web from a highly contaminated site, south China. Environ. Sci.

565

Technol. 44, 606-611.

566

Wu B., Liu S., Guo X. C., Zhang Y., Zhang X. X., Li M., Cheng S. P., 2012.

567

Responses of mouse liver to dechlorane plus exposure by integrative transcriptomic

568

and metabonomic studies. Environ. Sci. Technol. 46, 10758-10764.

569

Wu, C. W., Sun, J. Q., Zhang, A. P., Liu, W. P., 2013. Dissipation and

570

enantioselective degradation of plant growth retardants paclobutrazol and uniconazole

571

in open field, greenhouse, and laboratory soils. Environ. Sci. Technol. 47, 843-849.

572

Zeng, Y. H., Luo, X. J., Tang, B., Mai, B. X., 2016. Habitat- and species-dependent

573

accumulation of organohalogen pollutants in home-produced eggs from an electronic

574

waste recycling site in south China: Levels, profiles, and human dietary exposure.

575

Environ. Pollut. 216, 64-70.

576

Zheng, X. B., Wu, J. P., Luo, X. J., Zeng, Y. H., She, Y. Z., Mai, B. X., 2012.

577

Halogenated flame retardants in home-produced eggs from an electronic waste

578

recycling region in south China: Levels, composition profiles, and human dietary

579

exposure assessment. Environ. Int. 45, 122-128.

580

Zhang, A. P., Luo, W. X., Sun, J. Q., Xiao, H., Liu, W. P., 2015a. Distribution and

581

uptake pathways of organochlorine pesticides in greenhouse and conventional

582

vegetables. Sci. Total Environ. 505, 1142-1147.

AC C

EP

TE D

M AN U

SC

RI PT

559

24

ACCEPTED MANUSCRIPT Zhang, A. P., Liu, W. P., Yuan, H. J., Zhou, S. S., Su, Y. S., Li, Y. F., 2011. Spatial

584

distribution of hexachlorocyclohexanes in agricultural soils in zhejiang province,

585

China, and correlations with elevation and temperature. Environ. Sci. Technol. 45,

586

6303-6308.

587

Zhang, Y., Luo, X. J., Mo, L., Wu, J. P., Mai, B. X., Peng, Y. H., 2015b.

588

Bioaccumulation and translocation of polyhalogenated compounds in rice (Oryza

589

sativa L.) planted in paddy soil collected from an electronic waste recycling site, south

590

China. Chemosphere. 137, 25-32.

SC

RI PT

583

AC C

EP

TE D

M AN U

591

25

ACCEPTED MANUSCRIPT

1

Table 1 DP concentrations in soil, tomato and cucumber under different conditions (ng g-1 dw) Soil-BP

Soil-AP

Root

Stem

Leaf

Fruit Sample Soil-BP Soil-AP Root Stem Leaf Fruit Background soil TBG 3.4±0.29 3.6±0.30 1.2±0.11 2.8±0.21 1.5±0.17 2.1±0.41 TBC 3.5±0.33 3.3±0.22 1.2±0.11 2.5±0.21 1.2±0.081 1.3±0.42 CBG 3.3±0.21 3.5±0.25 1.5±0.17 2.6±0.27 1.4±0.11 2.3±0.31 CBC 3.3±0.28 3.1±0.19 1.4±0.10 2.1±0.19 1.1±0.10 1.8±0.48 Soil containing fresh DPs TFG-1 137±17 48±4.9 63±5.9 2.5±0.32 3.5±0.32 17±2.2 TFC-1 117±16 39±3.7 42±4.9 7.4±0.82 6.4±0.70 11±1.0 TFG-2 259±20 86±11 117±9.0 5.7±0.59 6.2±0.72 26±3.4 TFC-2 212±17 67±6.4 50±5.4 11±1.2 11±1.5 12±1.3 TFG-3 347±29 117±14 136±9.5 21±1.9 13±1.8 29±2.9 TFC-3 348±28 107±12 71±6.9 15±1.6 13±1.3 16±1.5 TFG-4 415±35 130±15 168±10 27±2.0 23±2.8 32±3.1 TFC-4 467±37 142±13 88±7.3 18±2.3 14±1.6 17±1.8 CFG-1 110±12 45±7.8 41±5.0 14±1.1 7.3±0.92 12±1.7 CFC-1 118±11 35±2.6 37±4.4 10±1.3 5.9±0.66 8.7±0.76 CFG-2 262±28 99±12 85±8.7 18±1.9 10±1.2 22±2.5 CFC-2 202±19 61±5.8 53±6.1 13±1.6 8.8±1.2 12±1.4 CFG-3 344±31 128±11 104±9.1 25±2.9 12±1.2 25±2.7 CFC-3 339±26 102±9.7 68±6.4 14±1.4 11±1.3 14±1.4 CFG-4 433±30 157±18 129±9.9 35±3.1 21±2.3 28±2.8 CFC-4 461±31 143±13 82±7.0 24±2.0 12±1.7 15±1.7 Soil containing aged DPs TAG-1 51±5.7 17±2.7 6.3±0.80 3.6±0.41 1.8±0.32 4.2±0.52 TAC-1 57±5.8 19±2.1 5.2±0.43 12±1.6 10±0.98 2.6±0.31 TAG-2 99±13 33±4.2 9.2±0.97 8.9±0.90 4.1±1.1 5.5±0.61 TAC-2 111±10 37±3.3 8.1±0.79 15±2.0 11±1.3 3.7±0.36 TAG-3 186±15 62±7.8 16±1.1 24±2.5 6.2±0.32 8.7±0.82 TAC-3 204±16 68±5.7 14±1.0 19±1.8 12±1.4 5.1±0.45 TAG-4 339±28 113±15 22±4.3 38±3.7 8.6±0.91 11±1.0 TAC-4 312±22 104±11 19±1.5 27±0.32 18±2.1 6.4±0.70 CAG-1 66±7.5 22±2.9 8.2±1.1 10±0.91 3.2±0.42 5.1±0.43 CAC-1 54±4.9 18±1.7 4.4±0.54 8.5±1.2 3.7±0.42 2.7±0.31 CAG-2 105±10 35±4.1 10±1.1 11±1.3 3.5±0.43 5.6±0.62 CAC-2 102±9.8 34±2.8 7.5±0.82 11±0.97 4.5±0.56 3.4±0.33 CAG-3 198±18 66±7.6 17±1.9 17±1.8 5.5±0.65 6.7±0.68 CAC-3 195±16 65±6.8 13±1.9 17±1.3 9.0±0.87 4.5±0.51 CAG-4 369±28 123±13 26±2.5 23±1.9 8.8±0.89 10±1.3 CAC-4 345±28 115±9.4 21±1.9 29±3.1 14±1.7 6.7±0.63 Soil-BP, DP concentration in soil before vegetables were planted; Soil-AP, DP concentration in soil after vegetables were planted. TBG and TBC: tomato planted in background soil in the greenhouse and the conventional open field, respectively; CBG and CBC: cucumber planted in background soil in the greenhouse and the conventional open field, respectively; TFG and TFC: tomato planted in soil containing fresh DP in the greenhouse and the conventional open field, respectively; TAG and TAC: tomato planted in soil containing aged DP in the greenhouse and the conventional open field, respectively; CFG and CFC: cucumber planted in soil containing fresh DP in the greenhouse and the conventional open field, respectively; CAG and CAC: cucumber planted in soil containing aged DP in the greenhouse and the conventional open field, respectively; The numbers (1, 2, 3, 4) represent four concentration levels.

2 3 4 5 6 7 8

AC C

EP

TE D

M AN U

SC

RI PT

Sample

ACCEPTED MANUSCRIPT

Table 2 fanti of DP in soil, tomato and cucumber under different conditions (ng g-1 dw) Root

Stem

Leaf

TBG CBG

0.74±0.06 0.75±0.04

0.72±0.08 0.71±0.01

0.69±0.08 0.72±0.07

0.73±0.07 0.75±0.05

0.72±0.08 0.67±0.11

TFG-1 TFG-2 TFG-3 TFG-4 CFG-1 CFG-2 CFG-3 CFG-4

0.71±0.08 0.74±0.06 0.77±0.03 0.70±0.08 0.77±0.04 0.75±0.04 0.71±0.07 0.70±0.07

0.74±0.03 0.74±0.05 0.71±0.07 0.72±0.05 0.72±0.03 0.79±0.03 0.75±0.04 0.77±0.01

0.73±0.04 0.76±0.06 0.74±0.03 0.69±0.05 0.73±0.05 0.75±0.06 0.73±0.08 0.78±0.02

0.75±0.03 0.78±0.05 0.70±0.05 0.69±0.06 0.76±0.03 0.74±0.01 0.76±0.03 0.75±0.01

0.68±0.06 0.71±0.04 0.68±0.07 0.72±0.04 0.72±0.06 0.73±0.04 0.73±0.06 0.72±0.06

TAG-1 TAG-2 TAG-3 TAG-4 CAG-1 CAG-2 CAG-3 CAG-4

0.74±0.05 0.71±0.04 0.70±0.07 0.72±0.06 0.69±0.07 0.75±0.04 0.72±0.06 0.67±0.09

0.76±0.03 0.75±0.06 0.72±0.03 0.78±0.01 0.73±0.03 0.74±0.04 0.72±0.03 0.71±0.05

0.74±0.06 0.72±0.03 0.74±0.05 0.76±0.01 0.70±0.06 0.70±0.05 0.74±0.05 0.73±0.03

0.75±0.03 0.76±0.04 0.71±0.07 0.72±0.06 0.75±0.04 0.74±0.05 0.72±0.05 0.71±0.04

0.76±0.03 0.67±0.09 0.69±0.06 0.73±0.03 0.66±0.11 0.75±0.04 0.74±0.03 0.75±0.02

Fruit Sample Soil-BP Background soil 0.68±0.09 TBC 0.73±0.04 0.67±0.10 CBC 0.72±0.03 Soil containing fresh DPs 0.68±0.09 TFC-1 0.74±0.05 0.70±0.05 TFC-2 0.75±0.03 0.69±0.07 TFC-3 0.77±0.03 0.72±0.05 TFC-4 0.74±0.06 0.77±0.03 CFC-1 0.74±0.03 0.79±0.01 CFC-2 0.73±0.04 0.76±0.03 CFC-3 0.76±0.03 0.72±0.01 CFC-4 0.71±0.07 Soil containing aged DPs 0.68±0.09 TAC-1 0.74±0.04 0.66±0.11 TAC-2 0.78±0.01 0.70±0.06 TAC-3 0.72±0.07 0.69±0.11 TAC-4 0.73±0.05 0.74±0.03 CAC-1 0.74±0.08 0.71±0.04 CAC-2 0.77±0.05 0.68±0.06 CAC-3 0.74±0.04 0.67±0.08 CAC-4 0.75±0.04

EP

AC C

Soil-AP

Root

Stem

Leaf

Fruit

0.77±0.03 0.78±0.01

0.72±0.06 0.76±0.05

0.70±0.05 0.69±0.09

0.73±0.03 0.78±0.03

0.74±0.07 0.78±0.04

0.74±0.07 0.72±0.04 0.71±0.06 0.75±0.04 0.74±0.05 0.76±0.02 0.74±0.06 0.72±0.03

0.76±0.03 0.78±0.03 0.76±0.02 0.72±0.09 0.75±0.03 0.71±0.06 0.72±0.05 0.73±0.05

0.74±0.03 0.71±0.08 0.72±0.05 0.70±0.06 0.72±0.03 0.71±0.05 0.74±0.06 0.72±0.07

0.67±0.10 0.66±0.11 0.70±0.03 0.69±0.08 0.68±0.13 0.70±0.06 0.69±0.08 0.68±0.08

0.72±0.06 0.69±0.07 0.71±0.05 0.70±0.06 0.71±0.07 0.75±0.05 0.69±0.08 0.68±0.07

0.75±0.07 0.74±0.08 0.76±0.03 0.77±0.03 0.74±0.06 0.73±0.02 0.76±0.03 0.78±0.01

0.76±0.03 0.72±0.04 0.77±0.03 0.75±0.04 0.77±0.04 0.72±0.04 0.78±0.03 0.77±0.04

0.71±0.04 0.74±0.05 0.75±0.08 0.71±0.04 0.72±0.03 0.75±0.02 0.76±0.07 0.73±0.07

0.77±0.03 0.70±0.12 0.74±0.07 0.68±0.11 0.67±0.07 0.75±0.03 0.66±0.10 0.69±0.09

0.74±0.03 0.73±0.05 0.70±0.03 0.69±0.05 0.68±0.15 0.67±0.15 0.69±0.08 0.66±0.10

RI PT

Soil-AP

SC

Soil-BP

TE D

Sample

M AN U

9

ACCEPTED MANUSCRIPT

10

Table 3 RSLCRs of vegetables cultivated under different conditions Soil-BP

Soil-AP

DP loss in soil

RSLCR

Sample

M AN U

89 173 230 285 65 163 216 276

TE D

48±4.9 86±11 117±14 130±15 45±7.8 99±12 128±11 157±18

EP

137±17 259±20 347±29 415±35 110±12 262±28 344±31 433±30

AC C

TFG-1 TFG-2 TFG-3 TFG-4 CFG-1 CFG-2 CFG-3 CFG-4

SC

Soil containing fresh DPs 0.71±0.066 TFC-1 0.68±0.052 TFC-2 0.59±0.041 TFC-3 0.59±0.45 TFC-4 0.63±0.077 CFC-1 0.52±0.053 CFC-2 0.48±0.042 CFC-3 0.47±0.036 CFC-4 Soil containing aged DPs Level 1 51±5.7 17±2.7 34 0.19±0.024 TAG-1 TAC-1 Level 2 99±13 33±4.2 66 0.14±0.015 TAG-2 TAC-2 Level 3 186±15 62±7.8 124 0.13±0.0089 TAG-3 TAC-3 339±28 113±15 226 0.097±0.019 Level 4 TAG-4 TAC-4 Level 1 66±7.5 22±2.9 44 0.19±0.025 CAG-1 CAC-1 Level 2 105±10 35±4.1 70 0.14±0.015 CAG-2 CAC-2 198±18 66±7.6 132 0.13±0.014 Level 3 CAG-3 CAC-3 Level 4 369±28 123±13 246 0.11±0.010 CAG-4 CAC-4 Abbreviations: RSLCRs: DP concentration in the root divided by the loss of DP concentration in the soil. Level 1 Level 2 Level 3 Level 4 Level 1 Level 2 Level 3 Level 4

11

Sample

Soil-BP

Soil-AP

DP loss in soil

RSLCR

117±16 212±17 348±28 467±37 118±11 202±19 339±26 461±31

39±3.7 67±6.4 107±12 142±13 35±2.6 61±5.8 102±9.7 143±13

78 145 241 325 83 141 237 318

0.54±0.063 0.34±0.037 0.29±0.029 0.27±0.022 0.45±0.053 0.38±0.043 0.29±0.027 0.26±0.022

57±5.8 111±10 204±16 312±22 54±4.9 102±9.8 195±16 345±28

19±2.1 37±3.3 68±5.7 104±11 18±1.7 34±2.8 65±6.8 115±9.4

38 74 136 208 36 68 130 230

0.14±0.011 0.11±0.011 0.10±0.0074 0.091±0.0072 0.12±0.015 0.11±0.012 0.10±0.015 0.091±0.0083

RI PT

Concentration level

ACCEPTED MANUSCRIPT Table 4 SBAFs, LBAFs and FBAFs of greenhouse and conventional vegetables planted in background soil TBG 0.78±0.060 0.42±0.051 0.58±0.11

TBC 0.76±0.060 0.27±0.020 0.39±0.13

CBG 0.78±0.080 0.42±0.030 0.75±0.090

CBC 0.68±0.059 0.35±0.031 0.48±0.15

AC C

EP

TE D

M AN U

SC

RI PT

Aerial part Stem Leaf Fruit

ACCEPTED MANUSCRIPT Table 5 TFs of DP in vegetables cultivated under different conditions TF

Soil containing fresh DPs 0.17±0.019 0.14±0.014 0.12±0.010 0.10±0.0082 0.15±0.020 0.12±0.013 0.10±0.011 0.093±0.0082 Soil containing aged DPs Level 1 TAG-1 0.056±0.0070 Level 2 TAG-2 0.048±0.0052 Level 3 TAG-3 0.052±0.0042 Level 4 TAG-4 0.038±0.0055 Level 1 CAG-1 0.064±0.0070 Level 2 CAG-2 0.047±0.0052 Level 3 CAG-3 0.033±0.0036 Level 4 CAG-4 0.031±0.0035 Abbreviations: TF: translocation factor. TFG-1 TFG-2 TFG-3 TFG-4 CFG-1 CFG-2 CFG-3 CFG-4

TF

TFC-1 TFC-2 TFC-3 TFC-4 CFC-1 CFC-2 CFC-3 CFC-4

0.12±0.013 0.073±0.0080 0.061±0.0058 0.048±0.0045 0.087±0.0089 0.074±0.0086 0.053±0.0051 0.042±0.0042

TAC-1 TAC-2 TAC-3 TAC-4 CAC-1 CAC-2 CAC-3 CAC-4

0.034±0.0034 0.032±0.0031 0.028±0.0022 0.024±0.0023 0.033±0.0040 0.028±0.0029 0.023±0.0030 0.023±0.0020

AC C

EP

TE D

M AN U

SC

Level 1 Level 2 Level 3 Level 4 Level 1 Level 2 Level 3 Level 4

Sample

RI PT

Concentration Sample level

ACCEPTED MANUSCRIPT Table 6 EDIs under different scenarios (ng d-1) EDI

Sample EDI Background soil GTb 14±2.7 CTb 8.5±2.8 GCb 7.8±1.0 CCb 6.1±1.6 Soil containing fresh DPs TFG-1 111±14 TFC-1 72±6.6 TFG-2 170±22 TFC-2 78±8.5 TFG-3 190±19 TFC-3 105±9.8 TFG-4 209±20 TFC-4 111±12 CFG-1 41±5.8 CFC-1 30±2.6 CFG-2 75±8.5 CFC-2 41±4.8 CFG-3 85±9.2 CFC-3 48±4.8 CFG-4 95±9.5 CFC-4 51±5.8 Soil containing aged DPs TAG-1 28±3.4 TAC-1 17±2.0 TAG-2 36±4.0 TAC-2 24±2.5 TAG-3 57±5.4 TAC-3 33±2.9 TAG-4 72±6.6 TAC-4 42±4.6 CAG-1 17±1.5 CAC-1 9.2±1.0 CAG-2 19±2.1 CAC-2 12±1.1 CAG-3 22±2.3 CAC-3 15±1.7 CAG-4 34±4.4 CAC-4 22±2.1 Abbreviations: EDI: estimated dietary intake.

AC C

EP

TE D

M AN U

SC

RI PT

Sample

ACCEPTED MANUSCRIPT Figure captions

AC C

EP

TE D

M AN U

SC

RI PT

Fig. 1 Half-lives of DP dissipation in greenhouse and open field (F, fresh DP; A, aged DP; s-DP, syn-DP; a-DP, anti-DP)

ACCEPTED MANUSCRIPT

120

Open field Greenhouse

RI PT

100

60

40

SC

Half-lives (d)

80

0 F s-DP

M AN U

20

F a-DP

A s-DP

A a-DP

Fresh and aged DPs in greenhouse and open field

Fig. 1 Half-lives of DP dissipation in greenhouse and open field (F, fresh DP; A, aged

AC C

EP

TE D

DP; s-DP, syn-DP; a-DP, anti-DP)

ACCEPTED MANUSCRIPT

Highlights (1) Greenhouse can enhance the uptake of DP by vegetables.

RI PT

(2) Greenhouse vegetables have higher levels of DP than conventional vegetables.

AC C

EP

TE D

M AN U

SC

(3) Higher exposure risk of DP was observed via greenhouse vegetables consumption.