Bulletin of Environmental Contamination and Toxicology (2018) 100:451–456 https://doi.org/10.1007/s00128-017-2237-9
Evaluation of Mercury Uptake and Distribution in Rice (Oryza sativa L.) Xiaoshuai Hang1,2 · Fangqun Gan2,3 · Yudong Chen1,2 · Xiaoqin Chen2 · Huoyan Wang2 · Changwen Du2 · Jianmin Zhou2 Received: 25 June 2017 / Accepted: 4 December 2017 / Published online: 11 December 2017 © Springer Science+Business Media, LLC, part of Springer Nature 2017
Abstract Mercury (Hg) contamination in soil-rice systems from industry, mining and agriculture has received increasing attention recently in China. Pot experiments were conducted to research the Hg accumulation capacity of rice under exogenous Hg in the soil and study the major soil factors affecting translocation of Hg from soil to plant. Soil treated with 2 mg kg−1 Hg decreased rice grain yield and inhibited the growth of rice plants. With increased Hg contamination of the rice, the enrichment rate of Hg was significantly higher in the rice grain than that in the stalk and leaf. Soil pH and cation exchange capacity are the key factors controlling Hg bioavailability in soils. Keywords Mercury · Rice tissues · Soil contamination · Oryza sativa L. · Enrichment rate Mercury (Hg) is a highly toxic contaminant worldwide. There has been an increasing focus on neurodevelopmental risk and neurotoxicity among people and animals exposed to even low doses of Hg (Davidson et al. 2004). Mining of nonferrous metals, coal combustion, smelting activities, industrial and agricultural uses of Hg, and sewage irrigation have led to increasing Hg accumulation in soils (Du et al. 2005). Wu et al. (2006) reported that nonferrous metals mining, coal combustion and smelting activities are three major sources of Hg pollution in China. According to recent national survey results of all kinds of soils in China, 1.6% of soil samples in survey sites nationwide exceed the acceptable limit of Hg in China (Shu et al. 2016). Contamination of soil and food crops is also an environmental and health concern because Hg can readily be taken up by plants and accumulated in the body where it poses a direct physiological threat to human health (Wang et al. 2012). As the world’s largest producer of rice (Oryza * Xiaoshuai Hang
[email protected] 1
Nanjing Institute of Environmental Science, Ministry of Environmental Protection of China, Nanjing, China
2
State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China
3
Department of City Science, The City Vocational College of Jiangsu (Jiangsu Open University), Nanjing, China
sativa L.), China accounts for 29% of the global rice yield (Rothenberg et al. 2012). As rice is the staple food for more than half of the world’s population, ingesting contaminated rice may pose a potential health risk to humans (Meng et al. 2014b). Rice is grown in flooded soil under reducing conditions. Like wetlands, rice fields are active sites for Hg methylation (Rothenberg et al. 2011). Recent study has shown that rice paddies, as a typical wetland ecosystem, are beneficial for methylmercury (MeHg) production and lead to elevated MeHg concentrations in the soil (Meng et al. 2010). Hurley et al. (1995) reported that under anaerobic conditions the mobility of Hg in soil solution can be enhanced and the methylation of Hg can be assisted by anaerobic microorganisms, thus enhancing the bioaccumulation of inorganic mercury (IHg) and MeHg in rice plants. Thus, several studies have confirmed that rice has higher accumulations of IHg and MeHg than other crops (Ren et al. 2014; Hang et al. 2016). Our previous result (Hang et al. 2016) indicated that IHg in rice grain was 2.55 times higher than that in wheat. Previous researches have mostly focused on Hg levels in rice and farm field soil, the risk of human exposure, and analyzing possible sources of Hg contamination. However, Hg in rice tissues can be enriched from the soil (Zhang et al. 2010), the ambient atmosphere (Meng et al. 2011), or a combination of these sources (Meng et al. 2012, 2014a). It was found that the relationship between Hg in rice grains and in the corresponding soil is not clear, because many factors
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Bulletin of Environmental Contamination and Toxicology (2018) 100:451–456
play roles in the transport of Hg from soil to grain, including soil pH and cation exchange capacity (CEC) (Wang et al. 2016), CaCO3 and organic materials (OMs) (Hang et al. 2016; Zuo et al. 2013), and redox conditions (Wang et al. 2014). The Hg bioavailability in soil reduces with the increase in contents of CEC, OMs, and CaCO3 (Hang et al. 2016). Previous report indicated that control of redox conditions will be an important role in reducing Hg accumulation in aerobically grown rice (Wang et al. 2014). In order to get more information on Hg enrichment in rice from the soil and its affecting factors, the goals of this study are: (1) to analyze the relationship between total Hg (THg) in rice tissues and soil; (2) to evaluate the accumulation capacity of rice under exogenous Hg in the soil; (3) to identify Hg accumulation in rice tissues associated with soil properties.
Materials and Methods The potted soils were collected from the surface layer (0–20 cm) of paddy soils in various farmlands surrounding Changshu City, Jiangsu Province. The soil samples were collected in November 2014, which was the rice harvest time. The field was dry during the time of collection. The rice grain was also collected from the corresponding field. There were nine soil samples for the pot experiments, all paddy soil formed on calcareous deposits of the Yangtze River. The soil was air dried and passed through a 2 mm nylon sieve. The physiochemical properties of the nine soil samples tested are listed in Table 1. The pH values of soil samples in this study ranged from 6.01 to 7.40 with an arithmetic mean of 6.42, corresponding to Grade I of the Environmental Quality Evaluation Standards for Farmland of Edible Agricultural Products (HJ332-2006). Soil OM values ranged from 1.19% to 4.42% with a mean of 2.92%, soil CEC ranged from
14.3 cmol kg−1 (+) to 24.0 with a mean of 19.8 cmol kg−1 (+), and CaCO3 ranged from 0.71% to 1.60% with a mean of 1.04%. Analysis of the Hg in the soil and the corresponding rice grain (brown grain) showed different levels of Hg in topsoil and rice grain (Table 2) (Hang et al. 2016): (I) concentrations of Hg in the soil were above the Chinese soil threshold level of 0.3 mg kg−1 (HJ332-2006), and the Hg level in the corresponding rice grain exceeded the maximum permissible Chinese limit of 20 µg kg−1 d.w. for crops (GB 2762-2005); (II) concentrations of Hg in the soil were above 0.3 mg kg−1, while the Hg level in the corresponding rice grain was below 20 µg kg−1 d.w., (III) concentrations of Hg in the soil were below 0.3 mg kg−1, while the Hg level in the corresponding rice grain exceeded 20 µg kg−1 d.w. The pot experiment was conducted to study the Hg uptake and distribution in rice. In order to go with the max observed, we chose the highest concentration (2.06 mg kg−1) of contaminated soil in field as the exposure concentration (2 mg kg−1) of experimental soil. There were two treatments of the nine soil samples: (1) Pot soil without added Hg as a Control (CK); (2) Pot soil treated with 2 mg kg−1 Hg (HT). Every soil had three replicates of each treatment, with 54 pots in the experiment. All soil was passed through a 2.0 mm mesh sieve. HT treatment soil was mixed with an appropriate amount of HgCl2. The untreated soil (CK) and the treated soil (HT) (3 kg) were each transferred into plastic pots (19 cm × 23 cm). Four seedlings were transplanted per pot in July 2015. Rice (Oryza sativa L.) was cultivated in the flooded pots with deionized water under greenhouse condition. The growth of the rice was observed and recorded. Compound fertilizer (N:P2O5:K2O = 9:15:15) was applied at a rate of 0.39 g kg−1 dry soil before rice planting. Additional fertilizer was added at 0.06 g kg−1 dry soil for N (urea) during the growing period. The rice was sown in July 2015 and harvested in November 2015.
Table 1 Physiochemical properties of the experimental soils
Soil
A
B
C
D
E
F
G
H
I
pH Soil organic matter (%) CEC cmol kg−1 (+) CaCO3 (%)
6.65 2.42 22.4 1.21
6.70 4.42 24.0 1.29
6.34 3.03 17.9 0.95
6.67 3.30 21.5 1.14
6.01 3.91 19.6 0.80
7.40 3.64 22.9 1.60
5.43 2.90 18.1 0.74
6.38 1.51 17.3 0.89
6.16 1.19 14.3 0.71
Table 2 Concentrations of Hg in the experimental soils and rice grain (field survey results)
Soil
Ia A
Hg in soil (mg kg−1) Hg in rice grain (µg kg−1)
II B
C
D
III E
2.06 0.94 0.48 0.77 1.38 31.1 47.9 50.4 11.3 7.5
F
Different levels of Hg in topsoil and rice grain
c
Threshold in China for Hg in soils (HJ332-2006)
Maximum permissible limit in China for Hg in crops (GB 2762-2005)
13
H
I
1.68 0.21 0.11 0.18 0.3b 14.5 26.0 36.0 60.2 20c
a
b
G
Limit value
After the rice was harvested, the samples of rice stalk and leaf, and grain (brown grain) were rinsed thoroughly with deionized water after ultrasonic cleaning, then dried in an oven at 80 °C, after 48 h to a constant weight. The dry weights (DWs) of the rice samples were determined, and the samples were crushed with a small grinder. The potted soil was air-dried at room temperature and ground, then passed through a 0.149 mm mesh sieve. Potted soil pH was determined using a pH meter (HI98182, Hanna Instruments, Italy). Soil OM was measured using the potassium dichromate oxidation method (Wang et al. 2016). Soil CEC was determined using the 1 mol L−1 NH4Cl–70%CH3CH2OH exchange method (Wang et al. 2016). For determination of total Hg, 1 g of soil sub-samples was digested with a mixed acid (V/V, 1:3:4 H NO3:HCl:H2O) (Shi et al. 2005). To determine Hg accumulated in plant tissues, rice stalk and leaf and grain samples (1 g) were digested in HNO3 and H2O2 (Han et al. 2006). The Hg content of all the digested solutions was analyzed using hydride generation atomic fluorescence spectrometry (AFS-930, Beijing Titan Instruments, China) (Fu et al. 2008), in which the detection limit for Hg was below 0.05 μg kg−1. Three parallels were conducted to analyze both soil and rice tissue samples. Reagent blanks, a standard reference soil sample (GBW07403), and standard rice and shrub branch and leaf samples (GBW10010 and GBW07602) were employed in the analysis to ensure accuracy and precision. The recovery rates of soil samples (GBW07403) and leaf samples (GBW10010 and GBW07602) were 92%–106% and 94%–108% for Hg, respectively. Statistical analyses were performed with the SPSS 22.0 statistical package. Correlation analysis was used to determine the relationships between Hg concentrations in soils and crops as well as soil properties. Statistical difference analysis was performed using One-way ANOVA to investigate significant levels of differences between CK and HT.
CK
a b
A
aa a
B
CK
4 2
b
1
b A
B
C
a
a
a
b
HT a
b
b
D E Soil
a
b
F
a
b
b
c
G
H
b I
Fig. 1 Soil Hg concentrations in different treatments after rice harvesting (Data are shown as mean ± SD, n = 3. Significant differences among data are indicated with different letter, p
