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Direct evidence of lead contamination in wheat tissues from atmospheric deposition based on atmospheric deposition exposure contrast tests
Ecotoxicology and Environmental Safety 185 (2019) 109688
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Direct evidence of lead contamination in wheat tissues from atmospheric deposition based on atmospheric deposition exposure contrast tests
T
Ma Chuanga,b,∗, Fu-Yong Liua, Bin Hua, Ming-Bao Weia,b, Ji-Hong Zhaob, Ke Zhanga,b, Hong-Zhong Zhangb,∗∗ a b
School of Materials and Chemical Engineering, Zhengzhou University of Light Industry, Zhengzhou, China Henan Collaborative Innovation Center of Environmental Pollution Control and Ecological Restoration, Zhengzhou University of Light Industry, Zhengzhou, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Wheat Soil Atmospheric deposition Pb Source apportionment
A field experiment was conducted to assess the atmospheric deposition effects on lead (Pb) contamination in wheat by two contrasting treatments: wheat exposed or not to atmospheric deposition. Plants were housed in a shed during wheat greening for the non-exposed treatment. The Pb contents of wheat during different growth stages, of soil and of atmospheric deposits were analysed and combined with Pb stable isotope data to quantify the contribution of atmospheric deposition and soil to Pb in wheat tissue. The Pb content in atmospheric deposits was significantly higher than those in soil and wheat tissue, and the Pb content in wheat tissue exposed to atmospheric deposition was significantly higher than the Pb content in non-exposed tissue (p < 0.05). The 206 Pb/207Pb of soil was significantly higher than the 206Pb/207Pb of atmospheric deposits (p < 0.05), and soil and atmospheric deposition were the two sources of Pb in wheat tissue. Atmospheric deposition was the main source of wheat tissue Pb in the exposed treatment, and most of the wheat tissue Pb, except for that in the stem, also came from atmospheric deposition in the maturing stage. The proportion of Pb from atmospheric deposition in roots, stems and leaves evidently decreased after the shed was erected, and the contribution of Pb from atmospheric deposition to wheat tissue was significantly higher in the exposed treatment than in the non-exposed treatment (p < 0.05). This contrast test directly confirmed that atmospheric deposition was the main source of Pb in the wheat tissues. Therefore, taking measures to reduce the absorption of Pb by wheat from atmospheric deposition can effectively ensure food safety.
1. Introduction Wheat is an important food crop that provides a basic source of food for humans. Many scholars have studied the relationship between the degree of Pb contamination in wheat grains and its ecological risk (Guo et al., 2018a; Murtaza et al., 2019). It is important to understand Pb contamination in wheat and to clarify the contribution of each pollution source to wheat Pb contamination to enable remediation (Belamri and Benrachedi, 2010; Ewing et al., 2010; Townsend and Seen, 2012). Pb generally enters wheat in two ways: the first is the absorption of Pb from soil by roots. Tong et al. (2018) studied the absorption and enrichment characteristics of Pb during wheat growth and found that with increasing soil Pb content, the enrichment coefficient decreased gradually. The reason for this difference is mainly the fact that the root system in the soil can be regarded as a barrier to the upward migration of Pb in plants (Townsend and Seen, 2012). The second way in which
∗
Pb enters wheat is the absorption of Pb from atmospheric deposits by aboveground plant parts. Yang et al. (2015) and Zhao et al. (2004) found that the leaves of cereal crops could absorb Pb from the atmosphere, suggesting that atmospheric deposition might be a source of Pb in grains. The Pb isotopic composition of matter is related to the characteristics of the Pb isotopic composition in only the source region (Li et al., 2017) and can be used to trace the source of Pb pollutants. To a certain extent, quantitative research can be carried out (Mirlean et al., 2005). Yang et al. (2015) used the Pb isotope technique to distinguish the sources of Pb in wheat grain and bran in the Beijing area in China and found that the content of Pb in soil was weakly related to the content of Pb in wheat grain. To a certain extent, atmospheric deposition may be an important source of Pb in wheat grain. However, to our knowledge, there is no direct experimental evidence that Pb in wheat originates from atmospheric deposition, and contrast testing has never been used
Corresponding author. Corresponding author. E-mail address: [email protected] (C. Ma).
∗∗
https://doi.org/10.1016/j.ecoenv.2019.109688 Received 23 May 2019; Received in revised form 9 September 2019; Accepted 15 September 2019 Available online 21 September 2019 0147-6513/ © 2019 Elsevier Inc. All rights reserved.
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analysis.
to study the source of Pb in wheat tissues exposed or not to atmospheric deposition. Therefore, we conducted a study in wheat fields in the suburbs of Zhengzhou, China, where plastic sheds were set up in farmland during the wheat greening period. Contrasting treatments of wheat exposed to atmospheric deposition (farmland inside the shed) and not exposed to atmospheric deposition (farmland outside the shed) were established. The contents of Pb and Pb stable isotopes in different tissues of wheat at different growth stages were analysed. The purposes of this study were 1) to study the effect of soil and atmospheric deposition on lead contamination of wheat, 2) to explore the distribution of Pb in wheat tissues exposed or not to atmospheric deposition during different growth stages, and 3) to quantify the effect of atmospheric deposition on Pb uptake by wheat and generate new ideas for controlling Pb contamination in wheat.
(III) Analysis methods For all analyses, each sample was run in triplicate. Sample analysis was carried out using an atomic absorption spectrometer (ZEEnit-700P, Analytik Jena, Germany). The wavelength used was 283.3 nm, the slit width was 1.2 nm, the current of the hollow cathode lamp (HCL) was 2.0 mA, the height of the burner was 6 mm, and the flow rate of acetylene was 65 L h−1 (Ai et al., 2016). For quality control, blank samples and nationally certified reference materials of soil (GBW07454) and plant material (GBW10046) were analysed. The recoveries of heavy metals in the soil and plant samples were within the allowable/acceptable range for nationally certified reference materials. The recovery of Pb in the standard plant samples was 105 ± 1.12% (85.0–115%), meeting the requirements of the national standard, and the recovery of Pb in the standard soil samples was 98.43 ± 2.65% (85.0–115%), meeting the requirements of the national standard. All reagents used in these experiments were super pure grades, and all glassware was soaked in an acid bath (concentrated nitric acid:water = 1:3) for 48 h. All samples prepared for Pb isotope analysis were sent to the Nuclear Industry Beijing Geological Research Institute for measurement using protocols outlined in the “Determination of the isotopic composition of trace Pb in rocks and minerals” (Chinese Standard DZ/T 0184. 12–1997) for hot surface ionization mass spectrometry. The isotope ratio of Pb was determined with reference to the standard substance SRM981 (Pb isotope reference material; American National Standards and Technology). Stable Pb isotopes in all samples were determined using an ISOPROBE-T thermal ionization mass spectrometer (GV Instruments Ltd, Manchester, UK). All samples were spotted on a sputum with silica gel, and Pb isotope ratios were measured in static mode.
2. Materials and methods 2.1. Sampling and analysis methods (I) Study area From March to July 2018, farmland in the northwestern suburb of Zhengzhou, Henan Province (China), was used as the study area (34°49′11″ N, 113°30′14″ E). The study area has a temperate monsoon climate and four distinct seasons, with rain and heat occurring in the same period and dry and cold in the same season. In this region, spring is dry and rainless, summer is hot and rainy, autumn is sunny with long daylight periods, and winter is cold, with less rain and snow. The annual average temperature is 14.3 °C, the hottest month is July with an average of 27 °C, the coldest is January with an average of 0.1 °C, and the average annual rainfall is 632 mm. The suitable temperature conditions, sufficient light and abundant rainfall in the crop growing season constitute good agrometeorological conditions (Fig. 1). During the greening period of winter wheat when the plant height reached 10 cm in March 2018, three experimental areas (3 m × 3 m) of wheat farmland were randomly selected as the non-exposed treatment; a 2 m tall shed was set up for the non-exposure test area, and a transparent plastic sheet covered the top of the shed. The screen (aperture of 1 mm) ensured isolation from the environment outside the shed and prevented atmospheric deposition. Three farmland areas of 3 m × 3 m around the three non-exposed treatment areas were selected for the atmospheric exposure treatment. Our winter wheat variety was Bainong Aikang 58, and the plant height was 60–70 cm at the mature stage. The roof of the shed was made of transparent plastic sheets, under which the greenhouse effect was easily produced. The temperature in the lower part of the shed was higher than the surrounding temperature by 1–2 °C. To reduce the effect of this temperature difference on the wheat plants, we made the height of the shed sufficiently high (2 m) allowed air circulation through gauze around the shed, thereby preventing a greenhouse effect in the shed.
2.2. Data statistics and processing The proportion of heavy metal isotopes in contaminated receptors is related to the natural composition of the heavy metal isotopes in only the pollution source and not to their migration behaviour or trajectory (Yang et al., 2015). Therefore, the use of Pb isotope tracers to identify sources of Pb pollution and related heavy metals in soil, the atmosphere and plants has become a powerful tool (Lin et al., 2018). Using Pb isotope “fingerprints”, Pb isotopes in wheat and the Pb isotope composition of soil and atmospheric deposits were detected (Wang et al., 2019a; Yang et al., 2015). According to the ratio of radioactive Pb isotopes, a linear mixing model was established to quantitatively calculate the contribution of soil and atmospheric deposition pollution sources to wheat contamination. The isotope ratios of the mixed sources in wheat plants, soil and atmospheric deposits were known, and the following formulas were established (Shiel et al., 2012).
(206Pb/207Pb) Soil × X + (206Pb/207Pb) Atmospheric .deposition × Y (II) Sampling methods
= (206Pb/207Pb)W heat
Wheat samples were collected at the greening stage (March 15), jointing stage (April 11), booting stage (May 6), filling stage (May 20) and mature stage (June 5) of wheat. When the wheat samples were collected, soil samples at depths of 0–20 cm were also collected, and atmospheric deposition samples were collected near the sampling site. To prevent disturbances from surrounding buildings and secondary deposition, samplers were installed on a telegraph pole taller than 4 m above ground level. Fifty millilitres of hexanediol was added to the samplers in advance to keep the samplers moist and to inhibit microbial and algal growth (Yang et al., 2015). After leaves and insects were removed from the samples, distilled water was added to wash out captured deposits. The samples were kept in a refrigerator before
X+Y=1
(1)
where X represents the soil contribution ratio and Y represents the atmospheric deposition contribution ratio. The significance of differences was evaluated with one-way analysis of variance (ANOVA) procedures followed by the LSD test. The significance level applied to all analyses was 5% (p < 0.05). All the data were analysed in SPSS 19.0 (SPSS Inc., Chicago, IL, USA) and described as the mean ± standard deviation (SD). The illustrations were created using Origin 9.0 (OriginLab., Northampton, Massachusetts, USA.)
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Fig. 1. Study area and sampling sites.
3. Results and analysis
not polluted, i.e., it was relatively clean soil. Based on the whole growth cycle of wheat, the content of Pb in wheat increased gradually at different stages but was lower during the grain filling period than during the other growth periods (Fig. 2). The content of Pb in different tissues of wheat at different growth stages showed a trend of roots > leaves > stems > wheat bran > grains. The content of Pb in roots, stems and leaves at the booting stage was higher than that at the greening stage, jointing stage, filling stage and mature stage (Fig. 2).
3.1. Pb content in wheat tissue, soil and atmospheric deposits The average Pb content was 5.78 ± 0.09 mg/kg in soil and 76.22 ± 1.454 mg/kg in deposits (Table 1). Compared with the second-class agricultural standard (80 mg/kg, pH > 7.5) of the soil environmental quality standard (GB 15618-1995), the regional soil was Table 1 Content of Pb in soil and atmospheric deposits (mg/kg).
Atmospheric deposits Soil (Non-exposed) Soil (Exposed)
Greening stage
Jointing stage
Booting stage
Filling stage
Mature stage
Mean
66.23 ± 0.016 a 5.10 ± 0.004 b 5.10 ± 0.004 b
79.87 ± 0.014 a 5.25 ± 0.012 b 5.74 ± 0.032 b
94.85 ± 0.020 a 5.74 ± 0.004 b 5.77 ± 0.008 b
65.58 ± 0.018 a 5.48 ± 0.010 b 5.96 ± 0.010 b
74.61 ± 0.025 a 6.09 ± 0.005 b 6.92 ± 0.024 b
76.22 ± 1.454 a 5.53 ± 0.064 b 5.90 ± 0.102 b
Note: The same letter (a, b) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test). 3
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Fig. 2. Pb content in wheat tissues in the exposed and non-exposed treatments. Note: Differences in the wheat tissues between the exposed and non-exposed treatments were analysed by the LSD test. Different letters (a, b) indicate that the values are significantly different at the P < 0.05 level.
et al., 2018), and the Pb isotope ratio of soil did not change over a short period of time (Chen et al., 2018; Evans et al., 2018). Therefore, in this study, mixed samples of exposed and non-exposed soils were used to determine the Pb isotope ratio, which did not affect the results (Li et al., 2017). The 206Pb/207Pb ratio of wheat tissue was between 1.1655 and 1.1799, and the ratio of Pb isotopes in wheat tissue was similar to that in soil at the greening, jointing and booting stages in both the nonexposed and exposed treatments. The ratio of lead isotopes in wheat tissues was more similar to that in atmospheric deposits at the grain filling and mature stages than at the greening, jointing and booting stages. The variation in the 206Pb/207Pb ratio (1.1724 ± 0.0015, 1.1685 ± 0.0023, 1.1687 ± 0.0022, 1.1670 ± 0.0028, 1.1740 ± 0.0001) (Table 2) of wheat was similar to that (1.1651 ± 0.0028) in atmospheric deposits in the exposed treatment. The variation in the 208Pb/206Pb ratio (2.0985 ± 0.0014, 2.0988 ± 0.0018, 2.0981 ± 0.0005, 2.1009 ± 0.0012, 2.0930 ± 0.0007) of wheat was more similar to that (2.1060 ± 0.0017) in atmospheric deposits in the exposed treatment than in the non-exposed treatment (Table 2). Some scholars have also confirmed that during wheat growth, the amount of heavy metals absorbed by roots and transported to stems and leaves is very small (Guo et al., 2018b), but the aboveground parts will gradually accumulate Pb over time, mainly due to atmospheric deposition. Choi et al. (2002) sprayed radioactive elements (54Mn, 134Cs and 57Co) on the surface of rice leaves and found that these ions were absorbed by leaves and transported to stems, grains and other organs. A
The content of Pb in atmospheric deposits was significantly higher than that in soil and wheat tissue at each stage of wheat growth (P < 0.05). A comparison of the two treatments indicated that the difference in the Pb content between the exposed treatment and the non-exposed treatment increased with the growth of wheat. The Pb content in the wheat tissue in the exposed treatment was higher than that in the non-exposed treatment, which indicated that the shed effectively prevented the absorption of Pb by wheat from atmospheric deposits and that atmospheric deposition was one of the sources of Pb in wheat tissues (Yang et al., 2015). 3.2. Pb isotope analysis of wheat tissue, soil and atmospheric deposits To quantify Pb in wheat tissue resulting from atmospheric deposition or soil, the Pb isotope ratios of soil, atmospheric deposits and wheat tissue were analysed. We quantified Pb sources in wheat tissue for source apportionment based on the 206Pb/207Pb ratio. The soil 206 Pb/207Pb (208Pb/206Pb) ratio was 1.1865 ± 0.0017 (2.0848 ± 0.0012), while that of atmospheric deposits was 1.1651 ± 0.0028 (2.1060 ± 0.0017) (Table 2). There were significant differences in the 206Pb/207Pb ratios between the soil and atmospheric deposits (p < 0.05). According to the Pb isotope composition and ratio relationships of different research objects, the source of pollutants can be determined, and quantitative research can be conducted (Mirlean et al., 2005). The soil samples were collected from wheat topsoil (0–20 cm), and although the Pb content of atmospheric deposits was high, the total amount of atmospheric deposition was very low (Zhang 4
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Table 2 Pb isotope ratios (206Pb/207Pb–208Pb/206Pb) in samples. Source
208
Soil Atmospheric deposits Wheat (Non-exposed)
2.0816–2.0873 2.0999–2.1098 2.0912–2.0946 2.0902–2.0987 2.0952–2.0993 2.0880–2.0987 2.0899–2.0909 2.0935–2.1010 2.0984–2.1043 2.0965–2.0993 2.0958–2.1017 2.0929–2.0932
Wheat (Exposed)
Roots Stems Leaves Bran Grains Roots Stems Leaves Bran Grains
Pb/206Pb
Pb/207Pb
Mean 2.0848 2.1060 2.0942 2.0933 2.0970 2.0923 2.0904 2.0985 2.0988 2.0981 2.1009 2.0930
± ± ± ± ± ± ± ± ± ± ± ±
0.0012 0.0017 0.0009 0.0017 0.0007 0.0022 0.0003 0.0014 0.0018 0.0005 0.0012 0.0007
206
Mean
1.1865–1.1891 1.1624–1.1709 1.1751–1.1799 1.1760–1.1784 1.1743–1.1783 1.1763–1.1794 1.1759–1.1791 1.1698–1.1754 1.1657–1.1734 1.1655–1.1720 1.1669–1.1741 1.1740–1.1741
1.1865 1.1651 1.1767 1.1765 1.1765 1.1780 1.1775 1.1724 1.1685 1.1687 1.1670 1.1740
± ± ± ± ± ± ± ± ± ± ± ±
0.0017 a 0.0028 f 0.0016 b 0.0006 b 0.0012 b 0.0011 b 0.0014 b 0.0015 cd 0.0023 e 0.0022 e 0.0028 de 0.0001 bc
Note: The same letter (a, b, c, d, e, f) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test).
stage, booting stage, filling stage and mature stage (Fig. 3f, R2 = 0.91) was 85.58%, 82.48%, 72.22%, 84.49%, and 92.79%, respectively. The contribution of non-exposed wheat leaves at the greening stage, jointing stage, booting stage, filling stage and mature stage (Fig. 3e, R2 = 0.93) was 42.48%, 41.39%, 59.75% and 59.04%, respectively. The contribution of atmospheric deposition to Pb in wheat leaves in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05). This finding is similar to the results of Yang et al. (2015), who used isotopes to explore wheat Pb sources, and of Schreck et al. (2014), who found that Pb in plant leaves was mostly derived from atmospheric deposition. Wheat bran is the closest part to the wheat grain, and the source of Pb in wheat bran also provides information on the source of Pb in wheat grain (He et al., 2000; Zhao et al., 2018). The binary linear mixed model of formula 1 showed that the contribution of deposition to Pb content in wheat bran at the booting stage, grain filling stage and mature stage of the exposed treatment was 83.12%, 94.71%, and 79.68%, respectively. The contribution of deposition to the Pb content in wheat bran of the non-exposed treatment was 43.44%, 39.78% and 53.13% at the booting stage, filling stage and mature stage (Fig. 3g, R2 = 0.87), respectively. The atmospheric deposition contribution in the exposed treatment was significantly higher than that in the nonexposed treatment (p < 0.05). This is consistent with the results of Yang et al. (2015), which confirms the significant contribution of atmospheric deposition. The 206Pb/207Pb ratios in wheat grains of the non-exposed treatment and exposed treatment were 1.1775 ± 0.0014 and 1.1740 ± 0.0001 (Table 3), respectively, which were significantly higher than that in soil (1.1651 ± 0.0028) and lower than that in atmospheric deposits (1.1865 ± 0.0017) (p < 0.05). The contribution of deposition to Pb in wheat during grain filling and at maturation in the exposed treatment (Fig. 3j, R2 = 0.91) was 60.79% and 79.89%, respectively, compared with the corresponding values of 52.28% and 54.68% in the non-exposed treatment (Fig. 3i, R2 = 0.98). The contribution of atmospheric deposition to wheat grain Pb in exposed areas was significantly higher than that in non-exposed areas (p < 0.05), which indicated that atmospheric deposition was the main source of Pb in grains, consistent with the results of Yang et al. (2015). In addition, the Pb content in wheat grains in the exposed treatment was significantly higher than that in the non-exposed treatment (Fig. 2), which verified that Pb on leaves was assimilated by leaf tissue and then transferred to the grain (Bi et al., 2009).
similar phenomenon was observed when Cakmak et al. (2000), who sprayed 109Cd solution on the surface of wheat leaves. 3.3. Source apportionment analysis of Pb in wheat tissues The line in Fig. 3 is the fitting line for the Pb isotope ratios in wheat tissue, soil and atmospheric deposits. The wheat tissue isotope ratio is located between the isotope ratios of soil and atmospheric deposits on the fitting line. Soil and atmospheric deposition can both be considered sources of Pb contamination in wheat tissue. The larger the R2 is, the more linear the isotope ratio of the three members. Wheat roots were located on the isotopic line between soil and atmospheric deposits (Fig. 3a and b). The use of formula 1 to analyse the binary linear mixing model indicated that the contribution of atmospheric deposition to the Pb content in wheat roots in the exposed treatment was higher than that in the non-exposed treatment. The effect of atmospheric deposition on the wheat Pb content in the grain filling and mature stages was higher than that in the wheat greening, jointing and booting stages (Table 3). Moreover, the contribution of atmospheric deposition to Pb in wheat roots in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05). It is generally accepted that wheat roots, being belowground tissues, are less affected by atmospheric deposition than the aboveground wheat tissues (Hansmann and Köppel, 2000; Qu et al., 2018). However, most of the Pb in wheat came from atmospheric deposition in the two treatments; this may be because wheat shoots absorb Pb from atmospheric deposits and transfer it to roots (Schreck et al., 2012). The contribution of atmospheric deposition to Pb in wheat stems in the exposed treatment in the greening stage, jointing stage, booting stage, grain filling stage and mature stage (Fig. 3d, R2 = 0.92) was 84.54%, 72.20%, 80.72%, 97.96%, and 84.04%, respectively. The contribution of atmospheric deposition to Pb in wheat stems in the nonexposed treatment was 84.54%, 54.10%, 44.56%, 43.73% and 42.01% in the greening stage, jointing stage, booting stage, grain filling stage and mature stage (Fig. 3c, R2 = 0.91), respectively. After the construction of the shed in the greening stage, the contribution of atmospheric deposition to the Pb in wheat stems in non-exposed treatment evidently decreased, from 84.54% in the greening stage to 42.01% in the mature stage. The influence of atmospheric deposition on the growth of wheat became increasingly obvious. The contribution of atmospheric deposition to Pb in wheat stems in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05), which indicated that atmospheric deposition was the main source of Pb in wheat stems (Wang et al., 2016; Yang et al., 2015). Leaves are the main tissues exposed to air and can absorb Pb directly from atmospheric deposits (Hu et al., 2011; Schreck et al., 2012). The binary linear mixed model of formula 1 showed that the contribution of deposition to wheat leaves in the greening stage, jointing
4. Discussion During the greening stage, transparent plastic sheeting was placed above wheat, and gauze was used to prevent atmospheric deposition to establish a contrast testing area for wheat without exposure to atmospheric deposition. After construction of the shed during the greening 5
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Fig. 3. Scatter plot of
206
Pb/207Pb–208Pb/206Pb for wheat tissue, soil and atmospheric deposits.
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Table 3 Contributions of soil and atmospheric deposition to the Pb content in wheat tissues. Region
Greening stage
Jointing stage
Booting stage
Filling stage
Mature stage
Medium
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
34.21% 15.46% 14.42% _ _ 34.21% 15.46% 14.42% _ _
65.79% 84.54% 85.58% _ _ 65.79% 84.54% 85.58% _ _
53.21% 55.90% 57.52% _ _ 41.19% 27.80% 17.52% _ _
46.79% 44.10% 42.48% _ _ 58.81% 72.20% 82.48% _ _
51.43% 55.44% 58.61% 56.56% _ 37.84% 19.28% 27.78% 16.88% _
48.57% 44.56% 41.39% 43.44% _ 62.16% 80.72% 72.22% 83.12% _
49.54% 56.27% 40.25% 60.22% 47.72% 30.25% 2.04% 15.51% 5.29% 39.21%
50.46% 43.73% 59.75% 39.78% 52.28% 69.75% 97.96% 84.49% 94.71% 60.79%
49.60% 57.99% 40.96% 46.87% 45.32% 28.97% 15.96% 7.21% 20.32% 20.11%
50.40% 42.01% 59.04% 53.13% 54.68% 71.03% 84.04% 92.79% 79.68% 79.89%
Wheat (Nonexposed)
Wheat (Exposed)
Roots Stems Leaves bran Grains Roots Stems Leaves bran Grains
d e f
c b a
e f g f d b c a
g h f i g d a c b e
h i e g f d b a c c
Notes: X represents the soil contribution ratio, and Y represents the atmospheric deposition contribution ratio. To satisfy the requirement of homogeneity of variance, the percentage data were transformed by arcsine function, and the angle was used for variance analysis. The same letter (a, b, c, e, f, g, h, i) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test).
growth period, but Pb was mainly enriched in wheat roots and leaves, similar to results reported by Al-Othman et al. (2012) and Tong et al. (2018). The Pb content in wheat roots, stems, leaves, grains and bran in the exposed area was higher than that in the non-exposed area; however, the difference in the Pb content between the exposed and nonexposed treatments was lower in wheat root tissue than in wheat stems, leaves, grains and bran. These results showed that the effect of Pb atmospheric deposition on wheat roots was relatively small, and the accumulation of Pb in wheat roots limited its transport to aboveground tissues (Puschenreiter et al., 2017). This may be because Pb that enters the roots is mainly stored in the cell wall in the form of ion-exchange carbonates, which bind with the carboxylated carbohydrates galacturonic acid and glucuronic acid, and the binding restricts the transport of Pb from roots to other tissues through ectoplasts (Sharma and Dubey, 2005).
period, the Pb content and the contribution of atmospheric deposition to wheat tissue Pb in the area exposed to atmospheric deposition were significantly higher than those in the area not exposed to atmospheric deposition (Fig. 2 and Table 3). This study provides a direct means to prove the effect of atmospheric deposition on Pb absorption in wheat for the first time. However, there are some limitations to this study. Most importantly, the plastic shed could not completely isolate small atmospheric deposits. The Pb isotope values also showed that a considerable part of the Pb in wheat tissue in the non-exposed areas was attributed to atmospheric deposition because the experimental shed in the farmland was surrounded by gauze with a pore size of 1 mm as a filter to ensure ventilation of the wheat in the shed. An attempt was made to maintain the natural temperature and water evaporation conditions to reduce the interference on wheat growth, and there are approximately 20%–60% PM2.5, PM10 and other fine particles in the atmospheric deposits of the Zhengzhou area (Jiang et al., 2018; Wang et al., 2017, 2019b). The filters surrounding the shed were unable to completely isolate small atmospheric deposits. Therefore, the next step should consist of indoor and outdoor comparative studies because growing wheat indoors completely excludes the impact of small atmospheric deposits while not interfering with wheat growth. This will be enable a more complete explanation of the effect of atmospheric dust on lead uptake by wheat. On the basis of the determined Pb contents, there was a significant difference between exposed and non-exposed wheat tissues grown in soils with the same background Pb content. The Pb content in wheat tissues in exposed areas was significantly higher than that in non-exposed areas. Therefore, it is inferred that the difference in Pb content in wheat tissues after exposure was mainly due to the accumulation and fixation of Pb in the aboveground tissues of wheat. Through isotopic tracer analysis, it was found that Pb in the atmosphere was mainly concentrated on wheat leaves. There are three ways for plant leaves to adsorb atmospheric particulates–retention (or stopping), attachment, and adhesion–and the mechanisms of the different adsorption modes are different (Prusty et al., 2005; Tallis et al., 2011). Through experimental findings and isotopic techniques, scholars found that Pb can enter wheat tissue through the leaves, and Shahid et al. (2016) and Uzu et al. (2010) confirmed this conclusion by using environmental scanning electron microscopy (ESEM-EDX) and Raman microspectroscopy (RMS). Generally, high accumulation of Pb occurs in organs with high metabolism, whereas nutrient storage organs such as seeds accumulate less Pb (Cairney and Meharg, 2002; Xie et al., 2016). During the whole growth process of wheat, the content of Pb in various tissues was ranked as roots > leaves > stems > wheat bran > grains (Fig. 2). The distribution of Pb in different tissues of wheat differed with the
5. Conclusions The Pb content and contribution of atmospheric deposits to Pb in wheat in the exposed treatment were significantly higher than those in the non-exposed treatment. After the construction of the shed, the Pb content of wheat and the contribution of atmospheric deposition to wheat Pb evidently decreased with the growth of wheat. Our study directly showed that wheat can absorb Pb in atmospheric deposits and that atmospheric deposition is the main source of wheat tissue Pb. Preventing atmospheric deposition can effectively control wheat grain Pb contamination. Acknowledgements This work was supported by grants from the National Natural Science Foundation of China (41501527; 41801086) and the Research Fund for the Doctoral Program of Zhengzhou University of Light Industry (2013BSJJ022). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoenv.2019.109688. References Ai, S., Guo, R., Liu, B., Ren, L., Naeem, S., Zhang, W., Zhang, Y., 2016. A field study on the dynamic uptake and transfer of heavy metals in Chinese cabbage and radish in weak alkaline soils. Environ. Sci. Pollut. Res. 23, 20719–20727. Al-Othman, Z.A., Ali, R., Al-Othman, A.M., Ali, J., Habila, M.A., 2012. Assessment of toxic metals in wheat crops grown on selected soils, irrigated by different water sources.
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Direct evidence of lead contamination in wheat tissues from atmospheric deposition based on atmospheric deposition exposure contrast tests
T
Ma Chuanga,b,∗, Fu-Yong Liua, Bin Hua, Ming-Bao Weia,b, Ji-Hong Zhaob, Ke Zhanga,b, Hong-Zhong Zhangb,∗∗ a b
School of Materials and Chemical Engineering, Zhengzhou University of Light Industry, Zhengzhou, China Henan Collaborative Innovation Center of Environmental Pollution Control and Ecological Restoration, Zhengzhou University of Light Industry, Zhengzhou, China
A R T I C LE I N FO
A B S T R A C T
Keywords: Wheat Soil Atmospheric deposition Pb Source apportionment
A field experiment was conducted to assess the atmospheric deposition effects on lead (Pb) contamination in wheat by two contrasting treatments: wheat exposed or not to atmospheric deposition. Plants were housed in a shed during wheat greening for the non-exposed treatment. The Pb contents of wheat during different growth stages, of soil and of atmospheric deposits were analysed and combined with Pb stable isotope data to quantify the contribution of atmospheric deposition and soil to Pb in wheat tissue. The Pb content in atmospheric deposits was significantly higher than those in soil and wheat tissue, and the Pb content in wheat tissue exposed to atmospheric deposition was significantly higher than the Pb content in non-exposed tissue (p < 0.05). The 206 Pb/207Pb of soil was significantly higher than the 206Pb/207Pb of atmospheric deposits (p < 0.05), and soil and atmospheric deposition were the two sources of Pb in wheat tissue. Atmospheric deposition was the main source of wheat tissue Pb in the exposed treatment, and most of the wheat tissue Pb, except for that in the stem, also came from atmospheric deposition in the maturing stage. The proportion of Pb from atmospheric deposition in roots, stems and leaves evidently decreased after the shed was erected, and the contribution of Pb from atmospheric deposition to wheat tissue was significantly higher in the exposed treatment than in the non-exposed treatment (p < 0.05). This contrast test directly confirmed that atmospheric deposition was the main source of Pb in the wheat tissues. Therefore, taking measures to reduce the absorption of Pb by wheat from atmospheric deposition can effectively ensure food safety.
1. Introduction Wheat is an important food crop that provides a basic source of food for humans. Many scholars have studied the relationship between the degree of Pb contamination in wheat grains and its ecological risk (Guo et al., 2018a; Murtaza et al., 2019). It is important to understand Pb contamination in wheat and to clarify the contribution of each pollution source to wheat Pb contamination to enable remediation (Belamri and Benrachedi, 2010; Ewing et al., 2010; Townsend and Seen, 2012). Pb generally enters wheat in two ways: the first is the absorption of Pb from soil by roots. Tong et al. (2018) studied the absorption and enrichment characteristics of Pb during wheat growth and found that with increasing soil Pb content, the enrichment coefficient decreased gradually. The reason for this difference is mainly the fact that the root system in the soil can be regarded as a barrier to the upward migration of Pb in plants (Townsend and Seen, 2012). The second way in which
∗
Pb enters wheat is the absorption of Pb from atmospheric deposits by aboveground plant parts. Yang et al. (2015) and Zhao et al. (2004) found that the leaves of cereal crops could absorb Pb from the atmosphere, suggesting that atmospheric deposition might be a source of Pb in grains. The Pb isotopic composition of matter is related to the characteristics of the Pb isotopic composition in only the source region (Li et al., 2017) and can be used to trace the source of Pb pollutants. To a certain extent, quantitative research can be carried out (Mirlean et al., 2005). Yang et al. (2015) used the Pb isotope technique to distinguish the sources of Pb in wheat grain and bran in the Beijing area in China and found that the content of Pb in soil was weakly related to the content of Pb in wheat grain. To a certain extent, atmospheric deposition may be an important source of Pb in wheat grain. However, to our knowledge, there is no direct experimental evidence that Pb in wheat originates from atmospheric deposition, and contrast testing has never been used
Corresponding author. Corresponding author. E-mail address: [email protected] (C. Ma).
∗∗
https://doi.org/10.1016/j.ecoenv.2019.109688 Received 23 May 2019; Received in revised form 9 September 2019; Accepted 15 September 2019 Available online 21 September 2019 0147-6513/ © 2019 Elsevier Inc. All rights reserved.
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analysis.
to study the source of Pb in wheat tissues exposed or not to atmospheric deposition. Therefore, we conducted a study in wheat fields in the suburbs of Zhengzhou, China, where plastic sheds were set up in farmland during the wheat greening period. Contrasting treatments of wheat exposed to atmospheric deposition (farmland inside the shed) and not exposed to atmospheric deposition (farmland outside the shed) were established. The contents of Pb and Pb stable isotopes in different tissues of wheat at different growth stages were analysed. The purposes of this study were 1) to study the effect of soil and atmospheric deposition on lead contamination of wheat, 2) to explore the distribution of Pb in wheat tissues exposed or not to atmospheric deposition during different growth stages, and 3) to quantify the effect of atmospheric deposition on Pb uptake by wheat and generate new ideas for controlling Pb contamination in wheat.
(III) Analysis methods For all analyses, each sample was run in triplicate. Sample analysis was carried out using an atomic absorption spectrometer (ZEEnit-700P, Analytik Jena, Germany). The wavelength used was 283.3 nm, the slit width was 1.2 nm, the current of the hollow cathode lamp (HCL) was 2.0 mA, the height of the burner was 6 mm, and the flow rate of acetylene was 65 L h−1 (Ai et al., 2016). For quality control, blank samples and nationally certified reference materials of soil (GBW07454) and plant material (GBW10046) were analysed. The recoveries of heavy metals in the soil and plant samples were within the allowable/acceptable range for nationally certified reference materials. The recovery of Pb in the standard plant samples was 105 ± 1.12% (85.0–115%), meeting the requirements of the national standard, and the recovery of Pb in the standard soil samples was 98.43 ± 2.65% (85.0–115%), meeting the requirements of the national standard. All reagents used in these experiments were super pure grades, and all glassware was soaked in an acid bath (concentrated nitric acid:water = 1:3) for 48 h. All samples prepared for Pb isotope analysis were sent to the Nuclear Industry Beijing Geological Research Institute for measurement using protocols outlined in the “Determination of the isotopic composition of trace Pb in rocks and minerals” (Chinese Standard DZ/T 0184. 12–1997) for hot surface ionization mass spectrometry. The isotope ratio of Pb was determined with reference to the standard substance SRM981 (Pb isotope reference material; American National Standards and Technology). Stable Pb isotopes in all samples were determined using an ISOPROBE-T thermal ionization mass spectrometer (GV Instruments Ltd, Manchester, UK). All samples were spotted on a sputum with silica gel, and Pb isotope ratios were measured in static mode.
2. Materials and methods 2.1. Sampling and analysis methods (I) Study area From March to July 2018, farmland in the northwestern suburb of Zhengzhou, Henan Province (China), was used as the study area (34°49′11″ N, 113°30′14″ E). The study area has a temperate monsoon climate and four distinct seasons, with rain and heat occurring in the same period and dry and cold in the same season. In this region, spring is dry and rainless, summer is hot and rainy, autumn is sunny with long daylight periods, and winter is cold, with less rain and snow. The annual average temperature is 14.3 °C, the hottest month is July with an average of 27 °C, the coldest is January with an average of 0.1 °C, and the average annual rainfall is 632 mm. The suitable temperature conditions, sufficient light and abundant rainfall in the crop growing season constitute good agrometeorological conditions (Fig. 1). During the greening period of winter wheat when the plant height reached 10 cm in March 2018, three experimental areas (3 m × 3 m) of wheat farmland were randomly selected as the non-exposed treatment; a 2 m tall shed was set up for the non-exposure test area, and a transparent plastic sheet covered the top of the shed. The screen (aperture of 1 mm) ensured isolation from the environment outside the shed and prevented atmospheric deposition. Three farmland areas of 3 m × 3 m around the three non-exposed treatment areas were selected for the atmospheric exposure treatment. Our winter wheat variety was Bainong Aikang 58, and the plant height was 60–70 cm at the mature stage. The roof of the shed was made of transparent plastic sheets, under which the greenhouse effect was easily produced. The temperature in the lower part of the shed was higher than the surrounding temperature by 1–2 °C. To reduce the effect of this temperature difference on the wheat plants, we made the height of the shed sufficiently high (2 m) allowed air circulation through gauze around the shed, thereby preventing a greenhouse effect in the shed.
2.2. Data statistics and processing The proportion of heavy metal isotopes in contaminated receptors is related to the natural composition of the heavy metal isotopes in only the pollution source and not to their migration behaviour or trajectory (Yang et al., 2015). Therefore, the use of Pb isotope tracers to identify sources of Pb pollution and related heavy metals in soil, the atmosphere and plants has become a powerful tool (Lin et al., 2018). Using Pb isotope “fingerprints”, Pb isotopes in wheat and the Pb isotope composition of soil and atmospheric deposits were detected (Wang et al., 2019a; Yang et al., 2015). According to the ratio of radioactive Pb isotopes, a linear mixing model was established to quantitatively calculate the contribution of soil and atmospheric deposition pollution sources to wheat contamination. The isotope ratios of the mixed sources in wheat plants, soil and atmospheric deposits were known, and the following formulas were established (Shiel et al., 2012).
(206Pb/207Pb) Soil × X + (206Pb/207Pb) Atmospheric .deposition × Y (II) Sampling methods
= (206Pb/207Pb)W heat
Wheat samples were collected at the greening stage (March 15), jointing stage (April 11), booting stage (May 6), filling stage (May 20) and mature stage (June 5) of wheat. When the wheat samples were collected, soil samples at depths of 0–20 cm were also collected, and atmospheric deposition samples were collected near the sampling site. To prevent disturbances from surrounding buildings and secondary deposition, samplers were installed on a telegraph pole taller than 4 m above ground level. Fifty millilitres of hexanediol was added to the samplers in advance to keep the samplers moist and to inhibit microbial and algal growth (Yang et al., 2015). After leaves and insects were removed from the samples, distilled water was added to wash out captured deposits. The samples were kept in a refrigerator before
X+Y=1
(1)
where X represents the soil contribution ratio and Y represents the atmospheric deposition contribution ratio. The significance of differences was evaluated with one-way analysis of variance (ANOVA) procedures followed by the LSD test. The significance level applied to all analyses was 5% (p < 0.05). All the data were analysed in SPSS 19.0 (SPSS Inc., Chicago, IL, USA) and described as the mean ± standard deviation (SD). The illustrations were created using Origin 9.0 (OriginLab., Northampton, Massachusetts, USA.)
2
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Fig. 1. Study area and sampling sites.
3. Results and analysis
not polluted, i.e., it was relatively clean soil. Based on the whole growth cycle of wheat, the content of Pb in wheat increased gradually at different stages but was lower during the grain filling period than during the other growth periods (Fig. 2). The content of Pb in different tissues of wheat at different growth stages showed a trend of roots > leaves > stems > wheat bran > grains. The content of Pb in roots, stems and leaves at the booting stage was higher than that at the greening stage, jointing stage, filling stage and mature stage (Fig. 2).
3.1. Pb content in wheat tissue, soil and atmospheric deposits The average Pb content was 5.78 ± 0.09 mg/kg in soil and 76.22 ± 1.454 mg/kg in deposits (Table 1). Compared with the second-class agricultural standard (80 mg/kg, pH > 7.5) of the soil environmental quality standard (GB 15618-1995), the regional soil was Table 1 Content of Pb in soil and atmospheric deposits (mg/kg).
Atmospheric deposits Soil (Non-exposed) Soil (Exposed)
Greening stage
Jointing stage
Booting stage
Filling stage
Mature stage
Mean
66.23 ± 0.016 a 5.10 ± 0.004 b 5.10 ± 0.004 b
79.87 ± 0.014 a 5.25 ± 0.012 b 5.74 ± 0.032 b
94.85 ± 0.020 a 5.74 ± 0.004 b 5.77 ± 0.008 b
65.58 ± 0.018 a 5.48 ± 0.010 b 5.96 ± 0.010 b
74.61 ± 0.025 a 6.09 ± 0.005 b 6.92 ± 0.024 b
76.22 ± 1.454 a 5.53 ± 0.064 b 5.90 ± 0.102 b
Note: The same letter (a, b) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test). 3
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Fig. 2. Pb content in wheat tissues in the exposed and non-exposed treatments. Note: Differences in the wheat tissues between the exposed and non-exposed treatments were analysed by the LSD test. Different letters (a, b) indicate that the values are significantly different at the P < 0.05 level.
et al., 2018), and the Pb isotope ratio of soil did not change over a short period of time (Chen et al., 2018; Evans et al., 2018). Therefore, in this study, mixed samples of exposed and non-exposed soils were used to determine the Pb isotope ratio, which did not affect the results (Li et al., 2017). The 206Pb/207Pb ratio of wheat tissue was between 1.1655 and 1.1799, and the ratio of Pb isotopes in wheat tissue was similar to that in soil at the greening, jointing and booting stages in both the nonexposed and exposed treatments. The ratio of lead isotopes in wheat tissues was more similar to that in atmospheric deposits at the grain filling and mature stages than at the greening, jointing and booting stages. The variation in the 206Pb/207Pb ratio (1.1724 ± 0.0015, 1.1685 ± 0.0023, 1.1687 ± 0.0022, 1.1670 ± 0.0028, 1.1740 ± 0.0001) (Table 2) of wheat was similar to that (1.1651 ± 0.0028) in atmospheric deposits in the exposed treatment. The variation in the 208Pb/206Pb ratio (2.0985 ± 0.0014, 2.0988 ± 0.0018, 2.0981 ± 0.0005, 2.1009 ± 0.0012, 2.0930 ± 0.0007) of wheat was more similar to that (2.1060 ± 0.0017) in atmospheric deposits in the exposed treatment than in the non-exposed treatment (Table 2). Some scholars have also confirmed that during wheat growth, the amount of heavy metals absorbed by roots and transported to stems and leaves is very small (Guo et al., 2018b), but the aboveground parts will gradually accumulate Pb over time, mainly due to atmospheric deposition. Choi et al. (2002) sprayed radioactive elements (54Mn, 134Cs and 57Co) on the surface of rice leaves and found that these ions were absorbed by leaves and transported to stems, grains and other organs. A
The content of Pb in atmospheric deposits was significantly higher than that in soil and wheat tissue at each stage of wheat growth (P < 0.05). A comparison of the two treatments indicated that the difference in the Pb content between the exposed treatment and the non-exposed treatment increased with the growth of wheat. The Pb content in the wheat tissue in the exposed treatment was higher than that in the non-exposed treatment, which indicated that the shed effectively prevented the absorption of Pb by wheat from atmospheric deposits and that atmospheric deposition was one of the sources of Pb in wheat tissues (Yang et al., 2015). 3.2. Pb isotope analysis of wheat tissue, soil and atmospheric deposits To quantify Pb in wheat tissue resulting from atmospheric deposition or soil, the Pb isotope ratios of soil, atmospheric deposits and wheat tissue were analysed. We quantified Pb sources in wheat tissue for source apportionment based on the 206Pb/207Pb ratio. The soil 206 Pb/207Pb (208Pb/206Pb) ratio was 1.1865 ± 0.0017 (2.0848 ± 0.0012), while that of atmospheric deposits was 1.1651 ± 0.0028 (2.1060 ± 0.0017) (Table 2). There were significant differences in the 206Pb/207Pb ratios between the soil and atmospheric deposits (p < 0.05). According to the Pb isotope composition and ratio relationships of different research objects, the source of pollutants can be determined, and quantitative research can be conducted (Mirlean et al., 2005). The soil samples were collected from wheat topsoil (0–20 cm), and although the Pb content of atmospheric deposits was high, the total amount of atmospheric deposition was very low (Zhang 4
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Table 2 Pb isotope ratios (206Pb/207Pb–208Pb/206Pb) in samples. Source
208
Soil Atmospheric deposits Wheat (Non-exposed)
2.0816–2.0873 2.0999–2.1098 2.0912–2.0946 2.0902–2.0987 2.0952–2.0993 2.0880–2.0987 2.0899–2.0909 2.0935–2.1010 2.0984–2.1043 2.0965–2.0993 2.0958–2.1017 2.0929–2.0932
Wheat (Exposed)
Roots Stems Leaves Bran Grains Roots Stems Leaves Bran Grains
Pb/206Pb
Pb/207Pb
Mean 2.0848 2.1060 2.0942 2.0933 2.0970 2.0923 2.0904 2.0985 2.0988 2.0981 2.1009 2.0930
± ± ± ± ± ± ± ± ± ± ± ±
0.0012 0.0017 0.0009 0.0017 0.0007 0.0022 0.0003 0.0014 0.0018 0.0005 0.0012 0.0007
206
Mean
1.1865–1.1891 1.1624–1.1709 1.1751–1.1799 1.1760–1.1784 1.1743–1.1783 1.1763–1.1794 1.1759–1.1791 1.1698–1.1754 1.1657–1.1734 1.1655–1.1720 1.1669–1.1741 1.1740–1.1741
1.1865 1.1651 1.1767 1.1765 1.1765 1.1780 1.1775 1.1724 1.1685 1.1687 1.1670 1.1740
± ± ± ± ± ± ± ± ± ± ± ±
0.0017 a 0.0028 f 0.0016 b 0.0006 b 0.0012 b 0.0011 b 0.0014 b 0.0015 cd 0.0023 e 0.0022 e 0.0028 de 0.0001 bc
Note: The same letter (a, b, c, d, e, f) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test).
stage, booting stage, filling stage and mature stage (Fig. 3f, R2 = 0.91) was 85.58%, 82.48%, 72.22%, 84.49%, and 92.79%, respectively. The contribution of non-exposed wheat leaves at the greening stage, jointing stage, booting stage, filling stage and mature stage (Fig. 3e, R2 = 0.93) was 42.48%, 41.39%, 59.75% and 59.04%, respectively. The contribution of atmospheric deposition to Pb in wheat leaves in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05). This finding is similar to the results of Yang et al. (2015), who used isotopes to explore wheat Pb sources, and of Schreck et al. (2014), who found that Pb in plant leaves was mostly derived from atmospheric deposition. Wheat bran is the closest part to the wheat grain, and the source of Pb in wheat bran also provides information on the source of Pb in wheat grain (He et al., 2000; Zhao et al., 2018). The binary linear mixed model of formula 1 showed that the contribution of deposition to Pb content in wheat bran at the booting stage, grain filling stage and mature stage of the exposed treatment was 83.12%, 94.71%, and 79.68%, respectively. The contribution of deposition to the Pb content in wheat bran of the non-exposed treatment was 43.44%, 39.78% and 53.13% at the booting stage, filling stage and mature stage (Fig. 3g, R2 = 0.87), respectively. The atmospheric deposition contribution in the exposed treatment was significantly higher than that in the nonexposed treatment (p < 0.05). This is consistent with the results of Yang et al. (2015), which confirms the significant contribution of atmospheric deposition. The 206Pb/207Pb ratios in wheat grains of the non-exposed treatment and exposed treatment were 1.1775 ± 0.0014 and 1.1740 ± 0.0001 (Table 3), respectively, which were significantly higher than that in soil (1.1651 ± 0.0028) and lower than that in atmospheric deposits (1.1865 ± 0.0017) (p < 0.05). The contribution of deposition to Pb in wheat during grain filling and at maturation in the exposed treatment (Fig. 3j, R2 = 0.91) was 60.79% and 79.89%, respectively, compared with the corresponding values of 52.28% and 54.68% in the non-exposed treatment (Fig. 3i, R2 = 0.98). The contribution of atmospheric deposition to wheat grain Pb in exposed areas was significantly higher than that in non-exposed areas (p < 0.05), which indicated that atmospheric deposition was the main source of Pb in grains, consistent with the results of Yang et al. (2015). In addition, the Pb content in wheat grains in the exposed treatment was significantly higher than that in the non-exposed treatment (Fig. 2), which verified that Pb on leaves was assimilated by leaf tissue and then transferred to the grain (Bi et al., 2009).
similar phenomenon was observed when Cakmak et al. (2000), who sprayed 109Cd solution on the surface of wheat leaves. 3.3. Source apportionment analysis of Pb in wheat tissues The line in Fig. 3 is the fitting line for the Pb isotope ratios in wheat tissue, soil and atmospheric deposits. The wheat tissue isotope ratio is located between the isotope ratios of soil and atmospheric deposits on the fitting line. Soil and atmospheric deposition can both be considered sources of Pb contamination in wheat tissue. The larger the R2 is, the more linear the isotope ratio of the three members. Wheat roots were located on the isotopic line between soil and atmospheric deposits (Fig. 3a and b). The use of formula 1 to analyse the binary linear mixing model indicated that the contribution of atmospheric deposition to the Pb content in wheat roots in the exposed treatment was higher than that in the non-exposed treatment. The effect of atmospheric deposition on the wheat Pb content in the grain filling and mature stages was higher than that in the wheat greening, jointing and booting stages (Table 3). Moreover, the contribution of atmospheric deposition to Pb in wheat roots in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05). It is generally accepted that wheat roots, being belowground tissues, are less affected by atmospheric deposition than the aboveground wheat tissues (Hansmann and Köppel, 2000; Qu et al., 2018). However, most of the Pb in wheat came from atmospheric deposition in the two treatments; this may be because wheat shoots absorb Pb from atmospheric deposits and transfer it to roots (Schreck et al., 2012). The contribution of atmospheric deposition to Pb in wheat stems in the exposed treatment in the greening stage, jointing stage, booting stage, grain filling stage and mature stage (Fig. 3d, R2 = 0.92) was 84.54%, 72.20%, 80.72%, 97.96%, and 84.04%, respectively. The contribution of atmospheric deposition to Pb in wheat stems in the nonexposed treatment was 84.54%, 54.10%, 44.56%, 43.73% and 42.01% in the greening stage, jointing stage, booting stage, grain filling stage and mature stage (Fig. 3c, R2 = 0.91), respectively. After the construction of the shed in the greening stage, the contribution of atmospheric deposition to the Pb in wheat stems in non-exposed treatment evidently decreased, from 84.54% in the greening stage to 42.01% in the mature stage. The influence of atmospheric deposition on the growth of wheat became increasingly obvious. The contribution of atmospheric deposition to Pb in wheat stems in the exposed treatment was significantly higher than that in the non-exposed treatment in the mature stage (p < 0.05), which indicated that atmospheric deposition was the main source of Pb in wheat stems (Wang et al., 2016; Yang et al., 2015). Leaves are the main tissues exposed to air and can absorb Pb directly from atmospheric deposits (Hu et al., 2011; Schreck et al., 2012). The binary linear mixed model of formula 1 showed that the contribution of deposition to wheat leaves in the greening stage, jointing
4. Discussion During the greening stage, transparent plastic sheeting was placed above wheat, and gauze was used to prevent atmospheric deposition to establish a contrast testing area for wheat without exposure to atmospheric deposition. After construction of the shed during the greening 5
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Fig. 3. Scatter plot of
206
Pb/207Pb–208Pb/206Pb for wheat tissue, soil and atmospheric deposits.
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Table 3 Contributions of soil and atmospheric deposition to the Pb content in wheat tissues. Region
Greening stage
Jointing stage
Booting stage
Filling stage
Mature stage
Medium
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
X (Soil)
Y (Atmospheric deposition)
34.21% 15.46% 14.42% _ _ 34.21% 15.46% 14.42% _ _
65.79% 84.54% 85.58% _ _ 65.79% 84.54% 85.58% _ _
53.21% 55.90% 57.52% _ _ 41.19% 27.80% 17.52% _ _
46.79% 44.10% 42.48% _ _ 58.81% 72.20% 82.48% _ _
51.43% 55.44% 58.61% 56.56% _ 37.84% 19.28% 27.78% 16.88% _
48.57% 44.56% 41.39% 43.44% _ 62.16% 80.72% 72.22% 83.12% _
49.54% 56.27% 40.25% 60.22% 47.72% 30.25% 2.04% 15.51% 5.29% 39.21%
50.46% 43.73% 59.75% 39.78% 52.28% 69.75% 97.96% 84.49% 94.71% 60.79%
49.60% 57.99% 40.96% 46.87% 45.32% 28.97% 15.96% 7.21% 20.32% 20.11%
50.40% 42.01% 59.04% 53.13% 54.68% 71.03% 84.04% 92.79% 79.68% 79.89%
Wheat (Nonexposed)
Wheat (Exposed)
Roots Stems Leaves bran Grains Roots Stems Leaves bran Grains
d e f
c b a
e f g f d b c a
g h f i g d a c b e
h i e g f d b a c c
Notes: X represents the soil contribution ratio, and Y represents the atmospheric deposition contribution ratio. To satisfy the requirement of homogeneity of variance, the percentage data were transformed by arcsine function, and the angle was used for variance analysis. The same letter (a, b, c, e, f, g, h, i) within the same column indicates that values are not significantly different at the P < 0.05 level (LSD test).
growth period, but Pb was mainly enriched in wheat roots and leaves, similar to results reported by Al-Othman et al. (2012) and Tong et al. (2018). The Pb content in wheat roots, stems, leaves, grains and bran in the exposed area was higher than that in the non-exposed area; however, the difference in the Pb content between the exposed and nonexposed treatments was lower in wheat root tissue than in wheat stems, leaves, grains and bran. These results showed that the effect of Pb atmospheric deposition on wheat roots was relatively small, and the accumulation of Pb in wheat roots limited its transport to aboveground tissues (Puschenreiter et al., 2017). This may be because Pb that enters the roots is mainly stored in the cell wall in the form of ion-exchange carbonates, which bind with the carboxylated carbohydrates galacturonic acid and glucuronic acid, and the binding restricts the transport of Pb from roots to other tissues through ectoplasts (Sharma and Dubey, 2005).
period, the Pb content and the contribution of atmospheric deposition to wheat tissue Pb in the area exposed to atmospheric deposition were significantly higher than those in the area not exposed to atmospheric deposition (Fig. 2 and Table 3). This study provides a direct means to prove the effect of atmospheric deposition on Pb absorption in wheat for the first time. However, there are some limitations to this study. Most importantly, the plastic shed could not completely isolate small atmospheric deposits. The Pb isotope values also showed that a considerable part of the Pb in wheat tissue in the non-exposed areas was attributed to atmospheric deposition because the experimental shed in the farmland was surrounded by gauze with a pore size of 1 mm as a filter to ensure ventilation of the wheat in the shed. An attempt was made to maintain the natural temperature and water evaporation conditions to reduce the interference on wheat growth, and there are approximately 20%–60% PM2.5, PM10 and other fine particles in the atmospheric deposits of the Zhengzhou area (Jiang et al., 2018; Wang et al., 2017, 2019b). The filters surrounding the shed were unable to completely isolate small atmospheric deposits. Therefore, the next step should consist of indoor and outdoor comparative studies because growing wheat indoors completely excludes the impact of small atmospheric deposits while not interfering with wheat growth. This will be enable a more complete explanation of the effect of atmospheric dust on lead uptake by wheat. On the basis of the determined Pb contents, there was a significant difference between exposed and non-exposed wheat tissues grown in soils with the same background Pb content. The Pb content in wheat tissues in exposed areas was significantly higher than that in non-exposed areas. Therefore, it is inferred that the difference in Pb content in wheat tissues after exposure was mainly due to the accumulation and fixation of Pb in the aboveground tissues of wheat. Through isotopic tracer analysis, it was found that Pb in the atmosphere was mainly concentrated on wheat leaves. There are three ways for plant leaves to adsorb atmospheric particulates–retention (or stopping), attachment, and adhesion–and the mechanisms of the different adsorption modes are different (Prusty et al., 2005; Tallis et al., 2011). Through experimental findings and isotopic techniques, scholars found that Pb can enter wheat tissue through the leaves, and Shahid et al. (2016) and Uzu et al. (2010) confirmed this conclusion by using environmental scanning electron microscopy (ESEM-EDX) and Raman microspectroscopy (RMS). Generally, high accumulation of Pb occurs in organs with high metabolism, whereas nutrient storage organs such as seeds accumulate less Pb (Cairney and Meharg, 2002; Xie et al., 2016). During the whole growth process of wheat, the content of Pb in various tissues was ranked as roots > leaves > stems > wheat bran > grains (Fig. 2). The distribution of Pb in different tissues of wheat differed with the
5. Conclusions The Pb content and contribution of atmospheric deposits to Pb in wheat in the exposed treatment were significantly higher than those in the non-exposed treatment. After the construction of the shed, the Pb content of wheat and the contribution of atmospheric deposition to wheat Pb evidently decreased with the growth of wheat. Our study directly showed that wheat can absorb Pb in atmospheric deposits and that atmospheric deposition is the main source of wheat tissue Pb. Preventing atmospheric deposition can effectively control wheat grain Pb contamination. Acknowledgements This work was supported by grants from the National Natural Science Foundation of China (41501527; 41801086) and the Research Fund for the Doctoral Program of Zhengzhou University of Light Industry (2013BSJJ022). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoenv.2019.109688. References Ai, S., Guo, R., Liu, B., Ren, L., Naeem, S., Zhang, W., Zhang, Y., 2016. A field study on the dynamic uptake and transfer of heavy metals in Chinese cabbage and radish in weak alkaline soils. Environ. Sci. Pollut. Res. 23, 20719–20727. Al-Othman, Z.A., Ali, R., Al-Othman, A.M., Ali, J., Habila, M.A., 2012. Assessment of toxic metals in wheat crops grown on selected soils, irrigated by different water sources.
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