Evaluation of various approaches to predict cadmium bioavailability to rice grown in soils with high geochemical background in the karst region, Southwestern China

Highlights

• The bioavailability of Cd in soils with high geochemical background was characterized as highly soil-type dependent.

• Soil Ca, pH, and total Cd are the controlling factors of Cd bioavailability.

• The DGT technique was a better approach to assess Cd bioavailability to rice.

• Derived regional soil threshold can prevent exceedance of Cd in rice.

Abstract

Evaluating the bioavailability of Cd to rice (Oryza sativa L.) was essential in the karst region, Southwestern China, where the soils have previously been shown to be anomalously enriched in Cd through geogenic processes. In this research, we examined the bioavailability of Cd to rice samples collected from 278 sites in Guangxi province, where rice is the most widely cultivated cereal crop that is responsible for the largest human dietary exposure to Cd. Both soil chemical extraction and soil-plant transfer modelling approaches were used to predict the bioavailability to rice. Some of the soil types were highly enriched in Cd, but their bioavailability was low, since the soil carbonates raised soil pH and remarkably reduced Cd bioavailability. In contrast, acidic soils (Ca was largely leached) with relatively low total Cd, the grown rice plants accumulated higher Cd in their grains. Results from CaCl₂ extraction experiments provided good predictions for Cd in rice grain grown in soils of different types. Stepwise multiple regressions revealed soil pH and soil Ca content were the dominant factors that control the transfer of Cd from soil to rice. An extended Freundlich-type model and a polynomial surface model provided good prediction for Cd in rice grains. The diffusive gradients in thin films (DGT) technique gave the best estimation of soil Cd bioavailability, whereas water-extracted soil solution Cd provided relatively poor fits. Regional soil threshold that derived using the models, can avoid exceedance of Cd in rice and thereby enable local agricultural practitioners or authorities to develop appropriate management for croplands with high Cd background.

Introduction

Cadmium (Cd), identified as the primary contaminant in Chinese agricultural land, is posing a severe threat to food safety and public health, due to the extensive Cd contamination in southern China (Wang et al., 2019b). Despite Cd contamination was mainly caused by the rapid industrial development and lack of sufficient environmental protection in China (Hu et al., 2016), the metal contaminations in southwest provinces (i.e. Guangxi, Yunnan, and Guizhou) may principally related to their high geochemical background (Chen et al., 2015). For instance, the background concentration of Cd in Guangxi (0.267 mg kg⁻¹) is much higher than the nationwide background (0.097 mg kg⁻¹) (CNEMC, 1990). The karst region in southwestern China, that is well known as one of the largest karst terrains in the world, has been reported with widespread Cd anomalies, that the Cd concentrations in the A and C soils were significantly higher in Guangxi and Guizhou province than in other regions of the country (Zhao et al., 2015).

Compared with other toxic elements, Cd can be more easily absorbed by edible plants from soils with a high transfer rate. The efficient soil-to-plant transfer of Cd, resulting in that cereals and vegetables accounts for approximately 90% of the Cd exposure among the non-smokers and for about 50% in the smoking population, since smokers inhale Cd in tobacco (Nicotiana tabacum L.), a hyperaccumulator of Cd (Clemens et al., 2013; Dai et al., 2017). For rice, it tends to accumulate more Cd than other cereals, so that rice as the most important regional cereal food in Guangxi is considered as the principal source of human dietary exposure to Cd, accounting for over 70% (Yu et al., 2017). Being a toxic and carcinogenic metal to humans, Cd exposure can lead to kidney damage and other adverse effects (Mao et al., 2019). The health risk through Cd exposure from rice is governed not only by its concentrations in rice grains, but also by their consumption rates (Meharg et al., 2013). For example, the rural residents from the remote areas of Guangxi have a much higher daily consumption of rice (493 g day⁻¹), compared with urban residents from the developed regions (137 g day⁻¹) (Li et al., 2012). It is thus urgent to accurately assess the Cd bioavailability to rice grown in the high Cd background area, where local population rely on rice for most of their caloric intake.

The potential mobility and bioavailability of Cd in soils with high geochemical background was usually low. For instance, Cd developed from Cd-enriched black shales in the Three Gorges Regions of China, exist mainly in the residual (mean at 41%) fraction and exhibited low mobility (Liu et al., 2017), while Cd in soils derived from carbonate rocks in Switzerland were principally associated with the carbonated fraction (mean at 49%), and also showed low lability unless under acidic condition (Quezada-Hinojosa et al., 2015). Yang et al. (2014) investigated the geochemical behaviors of trace metals (e.g. Ni, Cu, and Zn) in the soil-plant system in Guangxi, and reported that the bioavailability of these metals to plants is greatly lower in the soils derived from limestone, than that in soils from clasolite areas. The controlling factors of Cd bioavailability to vegetables in typical karst regions of Guangxi have previously been studied, which suggested that total soil Cd and pH were the critical influencing factors (Gan et al., 2018; Gan et al., 2017). However, the bioavailability of Cd and its uptake mechanisms by rice in the karst regions are still poorly understood.

Soil properties like pH, organic matter, and macronutrients (e.g. calcium, phosphorous, and iron) can control the Cd bioavailability (Li et al., 2017a,b; Sarwar et al., 2010). Chemical extractions (e.g. CaCl₂ extraction) were proved to be effective methods to evaluate Cd bioavailability (Houba et al., 2008; Zhang et al., 2010; Zhang et al., 2018b). Therefore, the relationships between the total or bioavailable Cd in soils, soil properties, and uptake amount of Cd by rice can be described with soil-plant transfer models based on linear regressions (Rodrigues et al., 2012; Römkens et al., 2009a). Additionally, it is recognized that Cd uptake by plants depends on not only Cd speciation in soils but also the dynamic processes of Cd resupply from the solid phase to soil solution (Tian et al., 2008). The DGT technique can measure the labile Cd concentrations including the dissolved fractions in soil solution and part of the resupplied fractions from the solid phase. As reported in previous studies, DGT technique showed a good performance to assess Cd bioavailability in soils (Luo et al., 2010; Williams et al., 2012; Zhang et al., 1998). More recently, the DGT technique has been reported to have higher capability of evaluating the Cd accumulation by plants in various soil types than traditional methods (Dai et al., 2017; Tian et al., 2018). The applicability of these methods in soils with high Cd background, to assess the bioavailability of Cd to rice, however has not been established yet.

Given the complex geological background, high variability of soil types and soil properties, and widespread Cd anomalies in the agricultural soils, in conjunction with the adequate dietary intake of rice for local population in the Guangxi karst region. The bioavailability of Cd to rice and its controlling factors in the soils need to be evaluated in this area. In this study, the follow aims were aspired: (i) characterize soil Cd bioavailability in soils with high geochemical background in the karst region (ii) understand the influence of soil properties on Cd bioavailability and Cd behavior in the soil-rice system (iii) assess the predictive capability of Cd accumulation in rice grains using various approaches, including the DGT technique, soil solution, chemical extraction, and soil-plant transfer models (iv) provide advice to improve local rice quality.