From soil to rice – a typical study of transfer and bioaccumulation of heavy metals in China

ABSTRACT

For the purpose of studying the contamination, bioaccumulation and transfer of heavy metals and understanding the effects of soil properties on these, the work was carried out on a regional scale. A total of 30 sets of soil and pairing rice tissues samples (root, straw and grain) were collected in Xiangzhou of Guangxi, China; soil properties and Cd, Cu, Pb and Zn of different rice tissues were analyzed. The mobility and bioaccumulation of Cd, Cu, Pb and Zn were assessed by transfer coefficients and bioaccumulation factors of them. The results indicated that the excess proportions of Cd and Pb were 50%, 3.33% and 30%, 6.67% in soil and rice grain, respectively, according to Chinese maximum permitted concentrations of heavy metals. Cd and Zn showed stronger bioaccumulation and mobility capability; the bioaccumulation and transfer of Cu were slightly lower than Cd and Zn; Pb had the weakest mobility. The bioaccumulation and mobility of heavy metals from soil to rice were restrained by soil pH, CaO, SOC, Fe oxides and Mn.

KEYWORDS:

• Heavy metal
• contamination
• transfer
• bioaccumulation

Introduction

Rice is one of the main crops in Xiangzhou, Guangxi known as granary in Guizhong Areas. The transfer and bioaccumulation of heavy metals from soil to rice are of great importance to human health, and rice cultivated in the pollution or high geological background of paddy soil can cause potential health problems (Wang et al. 2013; Kwon et al. 2017). Hence, heavy metals transfer and bioaccumulation in soil-rice system have become a hot topic.

With the development of urbanisation, industrialisation and the population growth, soil heavy metal pollution has caught worldwide attention in the last few decades due to its non- biodegradability and persistence in soils, which may cause environment pollution and human health problem (Sollitto et al. 2010; Luo et al. 2012; Gu et al. 2014; Zou et al. 2015; Kwon et al. 2017).

Heavy metals, one of the most primary types of contaminants, can be found in the tissues of plants, such as root, straw and grain (Zhao et al. 2010). Heavy metals uptake by plants roots and their transfer in soil-rice system were dominated by pH, cation exchange capacity, organic matter, plant species, and crop management practices (Cooper et al. 2011; Rodda et al. 2011; Zeng et al. 2011).

Consequently, the objectives of the present work are, (1) to examine Cadmium (Cd), Copper (Cu), Lead (Pb) and Zinc (Zn) concentrations of various rice tissues (root, straw and grain); (2) to evaluate the total metal bioaccumulation capacities of rice; (3) to discuss effects of soil pH, Soil Organic Carbon (SOC), CaO, Fe oxides and Mn on transfer and bioaccumulation of heavy metals (Cu, Cd, Pb and Zn). This work also provides scientific references to the assessment of ecological geochemistry, secure plan of land utilisation and government's new policy about the allocation of permanent basic farmland. The results will have a profound influence on the development of agriculture and economy of the studied area and provide scientific data for the environmental capacity and quality.

Materials and methods

Study area

The study was conducted in Xiangzhou city of Guangxi, located between 23°43′N-24°19′N and 109°25′E-110°06′E in south China. This area is located in the subtropical monsoon climate zone. The annual average temperature is 20.7°C, and the annual average rainfall is 1100–1700 mm. The topography of the entire area is dominated by hills. The exposure stratum contains mainly clastic rocks of Devonian, carbonates of Carboniferous, and sediments of Quaternary, which are given priority to carbonates of Carboniferous.

Sampling and preparation

Based on topographical features and rice distribution, rice roots, straws and grains and their topsoil samples were collected from the study area in the summer of 2015 year, shortly before harvesting (Figure 1). At each sampling site, three to five topsoil subsamples were gathered using a bamboo spade and mixed in a cotton bag. The sites where samples were taken are away from some obvious areas of human contaminations, i.e. roads, villages and garbage dumps. In the meantime, corresponding rice grain, straws and roots were collected with three to five subsamples and combined into a composite sample. After removing plant residues, debris and stones, the topsoil samples were air-dried thoroughly in the shade and sieved though a 10-mesh nylon sieve. The sieved topsoil samples were stored in clean polythene bags. Prior to analysis, about 200 g of topsoil samples were oven-dried below 40°C and ground to fine power (<0.074 mm) using an agate mortar for chemical analysis. The rice grain, straws and roots were carefully rinsed with tap water and then with deionised water, subsequently dried below 60°C to constant weight. Then root, straw and grain without husk were ground to a fine power (<0.25 mm) by stainless steel mill and kept in clean polythene bags for further chemical analysis (Yang et al. 2005).

Figure 1. Study area and sampling sites in Xiangzhou county of Guangxi.

Chemical analysis and quality control

According to soil sample analytical schemes (Ye, 2005; Zhang, 2005), pH and the concentrations of CaO, Fe oxides, Mn, Cd, Cu, Zn and Pb were analyzed. Soil pH was measured by ion selective electrode method. A volumetric method for the determination of SOC concentration in soil samples was applied. The contents of CaO, Fe oxides, Mn, Zn and Pb in the soil samples were tested with X-ray fluorescence spectrometry (XRF, PW2440, Philips Co., Dutch). To measure the concentrations of Cd and Cu, the soil samples were decomposed using HCl-HNO₃-HClO₄-HF. The concentrations of Cd and Cu were analyzed by inductively coupled plasma mass spectrometry (ICP-MS, Thermo Electron Co X-SERIES, America). The analytical data of soil properties were listed in Table 1.

Table 1. Descriptive statistics of soil chemical properties.

Soil properties	Mean	Maximum	Minimum	Standard deviation
pH	6.129	7.8	5.05	0.856
SOC /%	3.68	8.14	1.72	1.45
CaO /%	0.73	3.13	0.20	0.74
Fe oxides /%	4.73	11.13	1.70	2.32
Mn / mg·kg^−1	393.77	1145.00	87.00	292.06

Based on the National standard for food safety (GB 5009.268-2016) (National Health and Family Planning Commission of the People’s Republic of China, 2016), after the rice samples were digested by HNO₃ and H₂O₂, the concentrations of Cd, Cu, Pb, and Zn were determined by ICP-MS.

Chinese standardized reference materials (SRM) and internal and external duplicate samples were used to verify the analysis accuracy and precision. The accuracy and precision of the analysis of all samples were showed in Table 2.

Table 2. The accuracy and precision of the analyses (unit, %).

Soil			Root			Straw			Grain
Elements	RD	RE	Elements	RD	RE	Elements	RD	RE	Elements	RD	RE
Cd	7.4	8.04	Cd	–	4.12	Cd	–	4.52	Cd	5.4	6.28
Cu	2.58	1.81	Cu	–	8.37	Cu	–	6.83	Cu	2.49	8.05
Pb	4.3	3.32	Pb	–	8.6	Pb	–	7.34	Pb	1.25	8.91
Zn	1.49	2.75	Zn	–	7.47	Zn	–	7.97	Zn	2.83	8.37

Note: RD, relative duplicate difference; RE, relative error; -, no SRM.

Transfer coefficients (TCs) and bioaccumulation factors (BAFs)

To investigate the transfer and bioaccumulation of heavy metals from soil to rice, transfer coefficients (TCs) and bioaccumulation factors (BAFs) were determined.

The TCs were determined as the following (Green and Tibbett 2008),where C_isoil, C_iroot, C_istraw, and C_igrain represent the metal element ‘i’ s concentrations in the soil, root, straw and grain extracts, respectively.

BAF is defined as the ratio of heavy metal concentration in rice grain to that in soil, which roughly reflects the absorption capacity of a single heavy metal by rice grain (Chopra and Pathak 2015). The BAF was calculated using the following equations,where C _igrain, C _isoil means element ‘i’ content in rice grain and soil, respectively.

Statistical analysis and GIS methodology

Data was statistically analyzed using Microsoft Office Excel 2010 and GeoChemDAS 2.0.0. Box–whisker and scatter plots were created by using Grapher 8 and Microsoft Office Excel 2010, respectively. The sampling points were precisely defined by Global Positioning System (GPS) and the location and sample map and spatial distribution of heavy metal were produced using ArcGIS10.2 and CorelDRAW16 software.

Results

Concentrations of Cd, Cu, Pb and Zn in soil and rice

The concentrations of Cd, Cu, Pb and Zn in soil and various rice tissues are presented in Figure 2. In this study, the Cd, Cu, Pb and Zn concentrations ranged 0.10 ∼ 2.34, 11.40 ∼ 90.20, 16.00 ∼ 977.60 and 38.70 ∼ 201.60 mg kg⁻¹ in soil, 0.05 ∼ 4.70, 1.10 ∼ 20.11, 1.90 ∼ 245.79 and 16.67 ∼ 82.65 mg kg⁻¹ in root, 0.02 ∼ 2.17, 0.41 ∼ 2.87, 0.35 ∼ 19.74 and 5.63 ∼ 32.03 mg kg⁻¹ in straw and 0.01 ∼ 1.04, 0.71 ∼ 3.77, 0.07 ∼ 0.58 and 11.36 ∼ 19.07 mg kg⁻¹ in grain, respectively. The medium Cu, Pb and Zn concentrations in rice tissues were lower than those in soil, respectively; however, the medium Cd concentration in rice root was higher than that in soil. Generally, the medium concentrations of Cd, Cu, Pb and Zn in root were higher than those in straw and in grain, and these metals (except Cu) in straw were higher than those in grain.

Figure 2. Concentrations of Cd, Cu, Pb and Zn in soil and rice.

Transfer coefficients (TCs_root/soil) and bioaccumulation factors (BAFs)

According to Figure 3, the TCs of heavy metal elements from soil to root, root to straw, and straw to grain were gained and the transfer abilities were distinctly shown. The overall transfer capability was in the sequence of Cd > Zn > Cu > Pb in soil-root system; however, the transfer ability was in the sequence of Zn > Cd > Cu > Pb in root-straw systems and the order of Cu > Zn > Cd > Pb in straw-grain systems. The mean BAFs for Cd, Cu, Pb, and Zn were 0.424, 0.081, 0.002, and 0.191, respectively (Figure 3). In this study, the BAF of Pb was relatively low; nevertheless, the BAF of Cd was high compared with the BAF of Pb which was dozens of times to one hundred times of its. Based on the BAFs, the bioaccumulation ability in soil-rice grain system in the study area was in the sequence of Cd > Zn > Cu > Pb.

Figure 3. Transfer coefficients and bioaccumulation factors of Cd, Cu, Pb and Zn.

Correlations between soil properties and TCs and BAFs

In the current study, correlation relationship of Cd, Cu, Pb and Zn between soil properties and TCs were explictly shown in Figures 4–7. There were negative correlations between TCs of Cd, Cu, Pb and Zn and these soil properties. The significantly negative correlations between TC_{Cd root/soil} pH, CaO and SOC were strongly supported by Figure 4. The significantly negative correlations exited between TC_{Cu root/soil} and pH, CaO and Fe oxides and between TC_{Pb root/soil} and pH and CaO (Figures 5 and 6). Simultaneously, TC_{Zn root/soil} showed significantly negative correlations with pH, CaO, SOC, Fe oxides and Mn. Analogously, The BAF_{Cd grain/soil} values showed significantly negative correlations with pH, CaO, SOC and Mn (Figure 8); moreover, BAF_{Cu grain/soil} and BAF_{Zn grain/soil} were negatively correlated with pH, CaO, SOC, Fe oxides and Mn (Figures 9 and 10). In addition, the significantly negative correlations exited between BAF_{Pb grain/soil} and Cao, SOC, Fe oxides and Mn (Figure 11).

Figure 4. Scatter plot of TC_{Cd grain/soil} and soil properties.

Figure 5. Scatter plot of TC_{Cu grain/soil} and soil properties.

Figure 6. Scatter plot of TC_{Pb grain/soil} and soil properties.

Figure 7. Scatter plot of TC_{Zn grain/soil} and soil properties.

Figure 8. Scatter plot of BAF_{Cd grain/soil} and soil properties.

Figure 9. Scatter plot of BAF_{Cu grain/soil} and soil properties.

Figure 10. Scatter plot of BAF_{Zn grain/soil} and soil properties.

Figure 11. Scatter plot of BAF_{Pb grain/soil} and soil properties.

Discussion

Cd, Cu, Pb and Zn contaminations in soil and rice grain

Cd and Pb, two of the most harmful elements for plants and human beings, which could severely disturb plants’ respiration, photosynthesis, transpiration, and nutrient uptake(Gorinova et al. 2007; Krystofova et al. 2012; Zaidi et al. 2012); through the food chain of soil – plants – human beings, Cd and Pb can be a great threat to human health (Grimm et al. 2008; Wang et al. 2016). Although Cu and Zn were essential micronutrients for rice plants (Shahid et al. 2016), the excessive concentrations of Cu and Zn posed potential hazards for soil and rice. Excessive intake of Cd, Cu, Pb and Zn in the diet could cause impairment of kidney function, serious defects, abnormalities and other chronic toxicities (Chaney et al. 2004; Yeung and Hsu 2005).

The soil background concentrations of Cd, Cu, Pb and Zn are 0.144, 18, 24, and 43 mg kg⁻¹ in Guangxi, all of which were lower than the medium contents of them in soil samples. The concentrations of these metals are 0.31, 41.13, 48.30 and 137.03 mg kg⁻¹ in farmland of Zhengjiang (Zhao et al. 2010), and the concentrations of Cd and Pb were higher than their mean concentrations in soil samples of study area. According to the maximum allowable levels of Cd, Cu, Pb and Zn suggested by State Environmental Protection Administration of China (1995) (Table 3), the concentrations of some metals were higher than the maximum permitted contents. The excess portion of Cu, Cd and Pb were 6.67%, 50% and 3.33% in soil samples, respectively.

Table 3. Maximum allowable concentration of elements in paddy soil (unit: mg·kg⁻¹).

Elements	The division of pH values
	≤6.5	>6.5–7.5	>7.5
Cd	0.30	0.30	0.60
Cu	50	100	100
Pb	250	300	350
Zn	200	250	300

Some studies reported that Cd concentrations were the ranges of <1.0 and 0.03∼0.46 mg kg⁻¹ for rice grain grown on contaminated soil in Guangxi and Guangdong, China (Yang et al. 2006; Liu et al. 2011), respectively. For Pb, its concentrations ranged 0.004∼0.44 mg kg⁻¹ grown on contaminated soil in Korea (Park et al. 2011). In this study, Cd and Pb excess concentrations were also discovered in the rice grains. Of these rice grain samples, 30% contained Cd concentrations and 6.67% contained Pb concentrations above the allowable limits (0.2 mg kg⁻¹) specified by the maximum levels of contaminants in foods (Ministry of Health of China 2012).

Transfer and bioaccumulation of heavy metals

Transfer coefficients and bioaccumulation factors are significant parameters used to quantitatively describe uptake capacity of heavy metals in plants (Wang et al. 2012).

Generally, heavy metal concentrations in the various tissue types for rice decreased in the order of root > straw > grain (Liu et al. 2007; Liu et al. 2013), and however, Cu concentration decreased in the sequence of root > grain > straw in the present study (Figure 2), which showed stronger mobility of Cu from straw to grain than from root to straw. Combining with the transfer coefficients of heavy metal elements (Figure 3), we got that (1) it was easier for Cu and Zn to translocate from root to rice grain than for Cd and Pb; (2) transfer ability of Cd in soil-root system was stronger than that of other metals; (3) Pb had the weakest mobile ability from soil to rice.

BAF_{Pb grain/soil} was generally lower than 0.01, which was consistent with the results reported by Chen et al. (2016). According to Luo et al. (2011) and Li et al. (2012), the BAF of heavy metals can be used to evaluate the potential ability from soil to grain. Compared with other elements, the BAF_{Cd grain/soil} was significantly higher, with the average value of 0.42. Therefore, Cd had a higher capacity of being transferred from soils to rice grain. In general, other researchers revealed that Cd²⁺ with a higher biological absorption coefficient is more bioavailable to plant than Cu²⁺, Pb²⁺, and Zn²⁺ (Lee et al. 1998; Liu et al. 2007). Besides, higher concentrations of bio-accumulated Cd were observed when a higher concentration of Cd existed in the soil (Lanier et al. 2016), and soil Cd concentration was higher than other elements (Figure 2). BAF_{Zn grain/soil} was slightly lower than BAF_{Cd grain/soil}, with the average value of 0.19. According to Nan et al. (2002) and Chen et al. (2016), the synergy existed between Cd and Zn in soil–crop system.

Based on transfer coefficients and bioaccumulation factors, Cd and Zn exhibited stronger uptake capability in rice grain than Cu and Pb. Some papers reported that soil Cd primarily existed as exchangeable and bound to carbonates fractions (Wang et al. 2012), which could easily be absorbed by plant roots (Yang et al. 2009), and Zn²⁺ divalent cations could take up Cd²⁺ in plants by transporters (Welch and Norvell 1999; Chen et al. 2016); for Pb, residual and Fe/Mn oxides forms were primary in soil (Hou 2006), therefore soil Pb was not easily absorbed by rice. Though Cu exhibited stronger mobility from root to rice grain, the mobility of Cu from soil to rice root was limited in Cd contaminated soil. Some papers reported that Cd affected Cu concentration in root decreased significantly (Kashem and Kawai 2007); by competing with Cu for the same membrane transporters, Cd had an effect on uptake of Cu (Sarwar et al. 2010).

Effect of soil properties on TCs_root/soil and BAFs of heavy metals

Transfer and bioaccumulation abilities of heavy metals from soil to rice were mainly influenced by soil properties including pH, CaO, SOC, Fe oxides and Mn (Li et al. 2011; Jalali and Moradi 2013; Tahervand and Jalali 2016).

Soil pH showed significantly negative correlations with TCs_root/soil and BAFs of Cd, Cu and Zn (Figures 4–9 and Figure 10), indicating that soil pH restrained the uptake of Cd, Cu and Zn by rice root and grain and the increase of H⁺ promoted the transfer and bioaccumulation abilities of Cd, Cu and Zn from soil to root and grain, because the increase of H⁺ led to the decrease of the negative surface charge on soil as well as inhibited the adsorption of heavy metals to soil particles, and thus promote their release (Afkhami et al. 2010; Rajkumar et al. 2012). Moreover, soil pH showed the significantly negative correlation with TC_{Pb root/soil}, and however, there were no significant correlations between soil pH and BAF_Pb, illustrating that soil pH had a strongly negative effect on Pb transfer and a weakly negative influence on Pb bioaccumulation; this may be the result of Pb inhibition of transfer from root to grain.

CaO was significantly and negatively correlated with TCs_root/soil and BAFs of Cd, Cu, Pb and Zn (Figures 4–11), reflecting that CaO restrained the transfer and bioaccumulation of Cd, Cu, Pb and Zn, because Ca²⁺ could replace the Cd²⁺, Cu²⁺, Pb²⁺ and Zn²⁺ and also the use of CaO could elevate pH of soil solution resulting in the immobilisation of heavy metals caused by increased precipitation and sorption of heavy metals (Mahar et al. 2016).

There were significantly negative correlations between SOC and TCs_root/soil and BAFs of Cd and Zn (Figure 4 and Figures 7–11), showing that TCs and BAFs of Cd and Zn were inhibited by SOC, because Cd and Zn have similar chemical characters and SOC could absorb them onto soil constituents or forming stable complexes with humic substances (Garrett et al. 1998; Zarcinas et al. 2004; Santona et al. 2006; Antoniadis et al. 2008; Liu et al. 2009; Wang et al. 2012). In addition, SOC showed significantly negative correlation with BAFs of Cu and Pb, but was not significantly correlated with TCs_root/soil of Cu and Pb because the effect of SOC on bioaccumulation abilities of Cu and Pb concealed that on their transfer capabilities.

Furthermore, soil Fe oxides were significantly and negatively correlated with TCs_root/soil and BAFs of Cu and Zn (Figures 5, 7 and Figures 9–11), implying that soil Fe oxides restrained the transfer and bioaccumulation abilities of Cu and Zn in soil – rice system. Additionally, soil Fe oxides showed significantly negative correlation with BAF_Pb; however, it did not show significant correlation with TC_{Pb root/soil}, reflecting that the effect of soil Fe oxides on bioaccumulation ability of Pb hid that on its’ transfer capability. Similarly, soil Mn was significantly and negatively correlation with TC_{Zn root/soil} and BAFs of Cd, Cu, Pb and Zn (Figures 7–11), indicating that the transfer of Zn and bioaccumulation of Cd, Cu, Pb and Zn were inhibited by soil Mn, because the effects of soil Mn on TCs_root/soil of Cd, Cu and Pb were concealed those on BAFs of Cd, Cu and Pb.

Acknowledgments

The authors would like to thank Guangxi Geophysical Investigation Institute for assisting us in sampling and thank the anonymous reviewers for their critical reviews and constructive comments.

Disclosure statement

No potential conflict of interest was reported by the authors.

Notes on contributors

Qiubei Gu is a Ph.D. candidate at China University of Geosciences, Beijing, People’s Republic of China. She received her bachelor’s degree in China University of Geosciences, Beijing, People’s Republic of China. Her current work is focused on environmental geochemistry.

Zhongfang Yang is Professor at China University of Geosciences, Beijing, People’s Republic of China. She received her Master’s degree in Nanjing University, Nanjing, People’s Republic of China. Her current work is focused on environmental geochemistry, agricultural and ecological risk geochemical assessment.

Tao Yu is Associate Professor at China University of Geosciences, Beijing, People’s Republic of China. He received his Ph.D. in China University of Geosciences, Beijing, People’s Republic of China. His current work is focused on environmental geochemistry, agricultural and ecological risk geochemical assessment.

Qiong Yang is a Ph.D. candidate at China University of Geosciences, Beijing, People’s Republic of China. She received her bachelor’s degree in China University of Geosciences, Beijing, People’s Republic of China. Her current work is focused on environmental geochemistry.

Qingye Hou is Associate Professor at China University of Geosciences, Beijing, People’s Republic of China. She received her Ph.D. in China University of Geosciences, Wuhan, People’s Republic of China. Her current work is focused on environmental geochemistry, agricultural and ecological risk geochemical assessment.

Qizuan Zhang is Professor at Guangxi Bureau of Geology & Mineral Prospecting & Exploitation, Nanning, People’s Republic of China. He received his Ph.D. in China University of Geosciences, Beijing, People’s Republic of China. His current work is focused on geological survey and mineral exploration, marine geology and water drilling.

Additional information

Funding

This works were supported by the National Key R&D Program of China (grant number 2017YFD0800304), the project of Determination of Land Quality Geochemical Evaluation of Xiangzhou County in Guangxi, the Land and Resources Survey Project of China Geological Survey (grant number DD20160323) and the Fundamental Research Funds for the Central Universities (grant number 2652015433).