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Soil Contamination in China: Current Status and Mitigation Strategies Fang-Jie Zhao,*,†,‡ Yibing Ma,§ Yong-Guan Zhu,∥ Zhong Tang,† and Steve P. McGrath‡

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†

Jiangsu Key Laboratory for Organic Waste Utilization and National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Nanjing 210095, China ‡ Sustainable Soil and Grassland Systems Department, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, U.K. § Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China ∥ Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China S Supporting Information *

ABSTRACT: China faces great challenges in protecting its soil from contamination caused by rapid industrialization and urbanization over the last three decades. Recent nationwide surveys show that 16% of the soil samples, 19% for the agricultural soils, are contaminated based on China’s soil environmental quality limits, mainly with heavy metals and metalloids. Comparisons with other regions of the world show that the current status of soil contamination, based on the total contaminant concentrations, is not worse in China. However, the concentrations of some heavy metals in Chinese soils appear to be increasing at much greater rates. Exceedance of the contaminant limits in food crops is widespread in some areas, especially southern China, due to elevated inputs of contaminants, acidic nature of the soil and crop species or cultivars prone to heavy metal accumulation. Minimizing the transfer of contaminants from soil to the food chain is a top priority. A number of options are proposed, including identification of the sources of contaminants to agricultural systems, minimization of contaminant inputs, reduction of heavy metal phytoavailability in soil with liming or other immobilizing materials, selection and breeding of low accumulating crop cultivars, adoption of appropriate water and fertilizer management, bioremediation, and change of land use to grow nonfood crops. Implementation of these strategies requires not only technological advances, but also social-economic evaluation and effective enforcement of environmental protection law.

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INTRODUCTION

contaminants (hexachlorocyclohexane, dichlorodiphenyltrichloroethane, and polyaromatic hydrocarbons). Of all the samples analyzed, 16.1% exceed the environmental quality standard set by the MEP; for agricultural soils the percentage of exceedance is even greater at 19.4% (equivalent to approximately 26 million ha assuming that that the area is proportional to the number of survey samples). Contamination by heavy metals and metalloids (here, referring to the 8 elements listed in Table 1) accounts for the majority (82.4%) of the soils classified as being contaminated, with organic contaminants accounting for the rest. Among the heavy metals and metalloids, cadmium (Cd) ranks the first in the percentage of soil samples (7.0%) exceeding the MEP limit.

The status of soil contamination in China has attracted much public attention both domestically and internationally. The public concern arises largely from the scare about the safety of agricultural produce. Recently, the Ministry of Environmental Protection (MEP) and the Ministry of Land and Resources (MLR) of the People’s Republic of China issued a joint report on the current status of soil contamination in China.1 The report presents an overall grim situation with regard to the environmental quality of China’s soils. According to the report, soils in some areas, especially those surrounding mining and industry activities, have been seriously contaminated, while the quality of farmland soil is also of particular concern. The report is based on extensive surveys of soils conducted between 2005 and 2013, covering more than 70% of China’s land area. Surface (0−20 cm) soil samples were collected from 8 × 8 km grids and analyzed for 13 inorganic contaminants (arsenic, cadmium, cobalt, chromium, copper, fluoride, mercury, manganese, nickel, lead, selenium, vanadium, zinc) and 3 types of organic © 2014 American Chemical Society

Received: Revised: Accepted: Published: 750

September 25, 2014 December 11, 2014 December 16, 2014 December 16, 2014 DOI: 10.1021/es5047099 Environ. Sci. Technol. 2015, 49, 750−759

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Environmental Science & Technology

Table 1. Chinese Soil Environmental Quality Standards (Total Concentration in mg kg−1) and the Percentages of Soil Samples Exceeding the Class II Standards in the Recent National Soil Contamination Survey1,4 class II metal/metalloid Cd As paddy upland Hg Cu farmland orchard Pb Cr paddy upland Zn Ni a

class I (natural background)

pH 7.5

pH >6.5

% exceeding the limit

0.2

0.3

0.3

0.6

1.0

7.0

15 15 0.15

30 40 0.3

25 30 0.5

20 25 1.0

30 40 1.5

2.7a

35 35

50 150 250

100 200 300

100 200 350

400 400 500

90 90 100 40

250 150 200 40

300 200 250 50

350 250 300 60

400 300 500 200

1.6 2.1a 1.5 1.1a 0.9 4.8

The percentage exceedance is for all soil types.

trations of heavy metals and metalloids are not single values but are likely to vary substantially across the country. Natural background levels depend on the soil parent materials and pedogenetic processes, and therefore vary among different soil types.5−8 For example, soils developed from serpentine rocks are naturally enriched with nickel and chromium. The concentrations of several heavy metals are known to correlate closely with those of iron or aluminum oxides in soils, reflecting the parallel influences of pedogensis on these elements.5,9 A pan-European comparison revealed higher background levels of several heavy metals and metalloids in the more weathered soils of southern Europe than in the younger soils of northern Europe, with the break in concentrations coinciding with the maximum extent of the last glaciation.10 A national soil survey conducted in the early 1980s showed that the 90th percentile Cd concentrations in both the A and C soil horizons were markedly higher in Guizhou and Guangxi provinces in southwest China than in the other regions of China.11 Furthermore, soils developed from sedimentary parent materials, particularly sedimentary limestone, tend to have higher Cd concentrations than others.11 In the MEP/MLR soil contamination survey, soils with a high natural background of heavy metals or metalloids would also be classified as “contaminated”. Second, there are debates on whether the Class II values are overprotective or under-protective. Recent studies using soil to plant transfer models suggest that the Class II Cd limit may be set too low (i.e., overprotective) for soils with near neutral to alkaline pH.12,13 Certainly, the 0.3−0.6 mg kg−1 soil Cd limit (Table 1) is lower than either the 1−3 mg kg−1 limit adopted by the EU for land applications of sewage sludge or up to 39 mg kg−1 in the US-EPA’s rules on land applications of biosolids.14 The EU risk assessment on Cd has derived the predicted no effect concentrations (PNECs) of 0.6−2.3 mg kg−1 for the protection of human health, mammals and bird, plants and soil organisms,15 while the US-EPA recommends a screening value (ECOSSL) of 0.4−0.8 mg kg−1, above which further investigations are needed to determine if a site might be hazardous.16 In highly acidic soils, however, food Cd limits may be exceeded even when soil Cd concentrations are below 0.3 mg kg−1.13 On the other hand, there is some evidence that the Class II Pb limits may be set too high and may lead to

Arable land per capita in China is less than half of the world average, so protecting this precious resource from degradation and contamination has now been placed very high in the government’s agenda.2 Large sums of public funding have also been promised for the remediation of contaminated soils.3 However, how this should be done has been a subject of intense debate. Here, we present an appraisal of China’s current status of soil contamination and the effect on food safety, and propose strategies to deal with this worsening problem. The focus of this policy analysis is on heavy metals and metalloids in agricultural soils, as these can present a serious threat to human health through the food chain. Special emphasis is placed on Cd, as it is the most critical toxic metal threatening food safety and agricultural sustainability in China.

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SOIL QUALITY STANDARDS IN CHINA Because heavy metals and metalloids in soils are derived from both natural and anthropogenic sources, it is not straightforward to determine if a soil is contaminated. In the recent MEP/ MLR soil contamination survey, the status of soil contamination was determined by comparing the total concentration of a contaminant to the benchmark values of the Chinese environmental quality standard for soils issued by the MEP in 1995. The standard specifies three classes of benchmark values for eight heavy metals or metalloids and two pesticides4 (Table 1). Class I values are considered to represent the natural background, to be used in the protection of regional natural ecosystems from contamination. Class II is set up to protect agricultural production and human health via the food chain, and can be applied to agricultural, orchard and pasture land. The Class II values are dependent on soil pH and land use. In the recent MEP and MLR soil contamination survey, a soil is considered to be contaminated if a heavy metal or metalloid is above the class II value; the degree of contamination is designated as light, medium, or severe when the concentration is 1−3, 3−5, or >5 times the benchmark value, respectively. Class III is for the protection of crops or forests from phytotoxicity and may also be used where the natural background is elevated. A number of issues have been raised with regard to the China’s soil quality standards. First, for a country as large and geochemically diverse as China, natural background concen751

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Environmental Science & Technology noncompliance with the food Pb limits.17 The exposure pathway of soil ingestion by humans is also not considered in setting the Pb limits. Clearly, both issues would need to be addressed in any future revision of the soil quality standards in China, taking into account evidence accumulated since the standard was issued in 1995. When assessing the current status of soil contamination in China, it is important to bear in mind the assessment is relative to the magnitude of the benchmark values in the soil quality standard and some of the “contaminated” soils are because of naturally high background concentrations.

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THE CURRENT STATUS OF SOIL CONTAMINATION IN CHINA An important reason for the high percentages of Chinese soils identified as being contaminated with Cd (7%) is because of the low Class II values: 0.3 and 0.6 mg kg−1 for soils with pH 7.5, respectively (Table 1). Other countries may have higher Cd concentrations in their soils, compared with the recent soil survey results in China. For example, a national soil inventory shows that 45% and 20% of the soils in England and Wales exceed 0.3 and 0.6 mg kg−1, respectively.18 In continental Europe, the 75th percentile value of soil Cd was found to be 0.27 and 0.32 mg kg−1 for soils from agricultural and grazing land, respectively, 10 which means that a considerable proportion of European soils is over 0.3 mg kg−1 limit. In the US, the 75th percentile for agricultural areas was 0.34 mg kg−1.19 These comparisons help to place the current status of soil contamination in China in a different perspective: in terms of the total concentrations it is not worse than other regions such as Europe and the US. In the case of Ni, the relatively high percentage of contamination in China (4.8%, Table 1) is also due to, at least partly, the Class II values being set close to the Class I (natural background) level. On the other hand, the relatively low percentages of soil samples identified as being contaminated with Pb or Cr (Table 1) can be attributed to the large Class II values in the soil quality standard. While the current status of soil contamination in China may not be as grim as perceived in popular media, there are reasons for concern. This is because large quantities of heavy metals and metalloids have been discharged into the environment over the last three decades coinciding with rapid industrialization and urbanization in China. In 2012, 22 billion tons of wastewater, 64 trillion cubic meters of waste gas and 3.3 billion tons of solid waste were discharged from industrial sources in China.20 The total amount of five heavy metals and metalloids (Hg, Cd, Cr, Pb, and As) discharged in industrial wastewater reached 441 tons in 2012, although the discharge has been decreasing during recent years (Figure 1). The amounts of heavy metals released from mining are not quantified, but are probably substantially higher. In 2010, China consumed 3.38 billion tons of coal,21 which is likely to emit approximately 9000, 360, 450, and 25000 tons of As, Cd, Hg, and Pb, respectively, based on the average concentrations of these metals in coal and their emission factors.22 China is also the largest producer and consumer of many heavy metals in the world. For example, China produces and consumes about a third of the refinery cadmium in the world, most of it being used in the production of nickel−cadmium batteries.23 Uncontrolled discharges of wastewater, gas and solids have cumulatively raised the burden of heavy metals in the environment. A comparison between nationwide soil surveys conducted recently and those in the late 1980s shows clear

Figure 1. Discharge of heavy metals in industrial wastewater in China.20

increases in the total concentrations of a number of heavy metals and metalloids during the 25-year period. For example, average soil Cd concentrations increased by 10−40% in the western and northern China and by over 50% in the coastal region and the southwest of the country.24 Based on the inventory of inputs and outputs in agricultural systems not subjected to serious contaminations from point-sources, Luo et al.22 estimated that the Cd concentration in Chinese agricultural soils has been increasing at an average rate of 0.004 mg Cd kg−1 year−1. This is much greater than those reported elsewhere, e.g. 0.00033 mg Cd kg−1 year−1 in Europe,25 and would lead to a doubling of the average soil Cd concentration in China in 50 years if the input/output trend continued. Clearly, such an increase rate is worrying and must be reduced as soon and as much as possible. For comparison, it would take between 364 and 2433 years for the average concentrations of other heavy metals or metalloids in soil to increase from their background levels to the Class II limits.22 Therefore, Cd stands out as the most critical heavy metal for agricultural soils in China.

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HEAVY METALS AND METALLOIDS IN FOOD CROPS For heavy metals such as Cd to which the general population is exposed mainly through the food chain,25 keeping the metal concentrations in the edible parts of agricultural crops in check is an important and urgent task in China. An apparent paradox emerges when the soil-crop data in China and the UK are compared. While soil Cd concentrations in the UK are generally higher than those in China, wheat grain produced in the UK rarely exceeds the 0.2 mg Cd kg−1 limit of EU and FAO/WHO; exceedance was found in less than 0.2% of survey samples analyzed.26,27 In contrast, rice, the most important crop grown in southern China, appears to be problematic in meeting the 0.2 mg Cd kg−1 limit of the Chinese food standard. In some areas of southern China, particularly those impacted by mining and industrial activities, considerable proportions of rice grain exceed the Cd limit,28 causing widespread public concern in recent years. A recent survey of rice grain from a county located in the Xiangjiang river basin in Hunan province, one of the most important rice growing areas in China, showed that 60% of the samples exceed the 0.2 mg Cd kg−1 limit, and 11% contain >1.0 mg Cd kg−1.29 On a countrywide scale, market basket surveys reported between 2% and 13% of rice grain samples exceeding the limit.30−32 China has adopted a food standard limit of 0.2 mg Cd kg−1, which is stricter than the FAO/WHO’s limit of 0.4 mg kg−1 for 752

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concentrations in water of 5, 10, and 40 μg L−1 (these concentrations correspond to the drinking water limit, irrigation water limit and the highest concentration reported by Du et al.,29 respectively). These inputs could raise the Cd concentration in the topsoil (0−20 cm) by 0.02, 0.04, and 0.15 mg kg−1, respectively, in a single year if there were no losses of Cd from the system. On the basis of the typical biomass (12 tons ha−1 for grain and straw, respectively, for early and late rice) and the range of Cd concentrations in rice grain (0.05− 0.5 mg kg−1) and straw (0.4−4 mg kg−1) in southern China, crop uptake is likely to remove 5−55 g ha−1of Cd from the soil depending on the status of Cd contamination in the paddy field (Table 2), i.e. only about one tenth of the Cd inputs from

rice.33 This strict limit is deemed necessary because of the high consumption of rice by Chinese population: 238 and 327 g day−1 for national average and southern population average, respectively.34 Cd intake from rice alone with a Cd concentration of 0.2 mg kg−1 would amount to 0.73 and 1.01 μg kg−1 body weight day−1 for the national average (for adults of 65 kg body weight); the latter already exceeds the FAO/ WHO tolerable daily intake (TDI) of 0.83 μg kg−1 body weight day−1.35 For populations based on a subsistence rice diet, Cd in rice may pose a greater risk to humans because of the generally low concentrations of Fe and Zn in the diet, which could result in greater uptake of Cd,36 and such populations typically consume large amounts of rice (∼500 g day−1). Moreover, residents living in contaminated areas who consume mainly locally produced grain and vegetables are particularly vulnerable. A number of studies have shown that the dietary Cd intake for residents in some mining impacted areas in China is well over the TDI level, with rice being the most important source.37−40 In some cases the daily Cd intake exceeds 300 μg day−1 (4.6 μg kg−1 body weight day−1), which is likely to cause severe chronic Cd poisoning.41 There is also strong evidence linking elevated exposure to Cd with renal dysfunction and osteoporosis, and increased cancer mortality rate in populations impacted by mining activities in China.38,42−47 Apart from Cd, accumulation of As and Pb in rice is also of concern. A survey of rice grain collected from mining-impacted paddy fields in Hunan province showed that 65, 50, and 34% of the samples fail the national food standards for Cd, As, and Pb, respectively.28,48 Rice grain produced in a Hg mining and smelting area in Guizhou, southwest China, also contains significant amounts of methylmercury, a highly toxic species of Hg.49 Approximately a third of the local farmers in the area had a methylmercury intake exceeding the reference dose of 0.1 μg kg−1 bw day−1 established by the U.S. Environmental Protection Agency, with rice contributing to 95% of the intake.50

Table 2. Mass Balance of Cd in Double-Rice Cropping Systems in Southern China Cd outputs (g ha−1 yr−1)

Cd inputs (g ha−1 yr−1) irrigation (1 m water, 0.1−40 ppb Cd) phosphate fertilizers organic manures atmospheric deposition (mean) a

1−400 0.04−2 0−10 0.4−25(4)

rice uptake leaching runoff

5−55 NDa NDa

ND, no data available.

irrigation water. There are other sources of heavy metals and metalloids, such as atmospheric deposition, fertilizers and manures (Table 2). Due to metal smelting and coal combustion, the rates of atmospheric deposition in China are higher than those in developed countries.22 Atmospheric deposition of Cd ranges from 0.4 to 25 g ha−1 year−1 in China with a mean of 4 g ha−1 yr−1,22 which is substantially higher than the current mean of EU of 0.35 g ha−1 yr−1.53 Phosphate fertilizers can contain considerable amounts of Cd. But fortunately, many rock phosphates in China have low levels of Cd and consequently, home-produced phosphate fertilizers are not an important source of Cd to agricultural soils, although some imported phosphate fertilizers used to make compound fertilizers may be elevated in Cd.22,54 Some organic manures contain high levels of heavy metals or metalloids, especially Zn, Cu, As and occasionally, Cd.22 Where sewage sludge is applied onto agricultural land, it could also add significant amounts of heavy metals, especially Zn and Cu.22 The data for losses of heavy metals through runoff and leaching are scarce, making mass balance calculations difficult. However, it is apparent from Table 2 that irrigation is the dominant source of Cd in the double rice cropping system in southern China if the water used contains elevated levels of Cd. The second important reason causing high accumulation of cationic heavy metals in rice and vegetables is the acidic nature of the soils in many areas of southern China, leading to a high phytoavailability of Cd in the soil. In the tropical and subtropical regions of southern China, red soil and the paddy soil developed from this soil type are inherently acidic. Use of acidifying nitrogen fertilizers, crop uptake of base cations and acid deposition from the atmosphere have contributed to significant soil acidification in major croplands in China over the last three decades.55 Approximately half of the paddy soils in Hunan province have a pH lower than 5.5. Several field or pot studies have shown that paddy soil pH has a highly significant effect on the accumulation Cd in rice grain.13,56,57 Based on the regression model presented by Römkens et al.,56 it can be predicted that for Indica rice cultivars which are

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CAUSES OF HEAVY METAL CONTAMINATION IN SOILS AND FOOD CROPS IN SOUTHERN CHINA Exceedance of heavy metal limits in food crops is more common in southern China than in other regions for a number of reasons. First, mining of base metals and metal smelting have been important economic activities in some parts of southern China for a long time. These activities have released large quantities of heavy metals and metalloids into the environment because of the inadequate enforcement of environmental protection law. Taking Hunan province (the largest rice producing province in China) as an example, it has been estimated that mining, smelting and other industries released 610, 31, 136, and 4 tons year−1 of Pb, Cd, Cr, and Hg, respectively, into the Xiangjiang river, a major tributary of the Yangtze River.51 Xiangjiang river basin is an important rice producing area, but is also among the most contaminated areas in China.52 Some streamwater in the Xiangjiang River catchment area contains as much as 40 μg Cd L−1, 8 times the drinking water limit,29 while Liu et al.51 reported maximum concentrations of 430 μg Cd L−1, 500 μg As L−1, and 138 μg Pb L−1 in some sections of Xiangjiang river. As the double-rice cropping system, a typical cropping system in southern China, consumes large quantities irrigation water, inputs of heavy metals into the soil can be substantial. Assuming 1 m irrigation water per year, the input of Cd into the paddy system would amount to 50, 100, and 400 g ha−1, respectively, with Cd 753

DOI: 10.1021/es5047099 Environ. Sci. Technol. 2015, 49, 750−759

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Environmental Science & Technology commonly grown in southern China, grain Cd may exceed the 0.2 mg kg−1 limit when soil Cd concentration is above 0.18 and 0.9 mg kg−1 at soil pHs of 5 and 7, respectively (Figure 2). This

On the basis of the regression models developed for the average Indica and Japonica rice,56 it is clear that Indica rice is more likely to exceed the grain Cd limit than Japonica rice; for the latter exceedance is predicted with a soil total Cd of 0.55 and 1.7 mg kg−1 at pH 5 and 7, respectively (Figure 2). On acidic soils, some vegetables, such as carrot, leafy, brassica and solanaceous vegetables, are also prone to Cd accumulation,13,68−70 therefore adding to the dietary Cd intake of the local residents.70−72 So, the combination of soil contamination, high phytoavailability in acidic soils and cultivation of heavy metal accumulating rice cultivars and vegetable species substantially increases the risk of the transfer of heavy metals from soil to the food chain in southern China. Under these conditions, naturally elevated concentrations of heavy metals may pose a risk similar to those from anthropogenic activities. The last two factors discussed above probably also explain why such risk is higher in southern China than in Europe at the same level of total metal concentration in soil.

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STRATEGIES TO MITIGATE HEAVY METAL CONTAMINATION IN FOOD CROPS Urgent measures are needed to mitigate the serious problem of heavy metal or metalloid contamination in food crops in China, some of which are discussed below. Implementation of various strategies requires not only technological advances, but also social-economic evaluation and effective enforcement of environmental protection law, as well as government subsidy. Identify and Stop the Sources of Contamination. The first step to combat heavy metal contamination in the soil-plant systems is to identify and stop the main sources of contamination. This requires more stringent monitoring and effective enforcement of environmental protection law, especially with regard to large emission sources such as mining, smelting and other metal consuming industries. There is an urgent need to establish national and regional inventories of metal and metalloid concentrations in water used for irrigation and of atmospheric inputs. This would enable realistic appraisal of the current contamination status and prediction of the future trend. Where irrigation water contains elevated levels of metals or metalloids, simple and effective techniques should be developed to remove the contaminants before water reaches the field; where this is not possible, alternative clean water sources would need to be found. Starting in 2011, the Chinese government has initiated two large national programs to combat heavy metal pollution: the 12th five-year plan for preventing heavy metal pollution and the Xiangjiang river basin control plan for heavy metal pollution, each with funding of tens of billions of Chinese Yuan.52 The first program aims to strengthen the control and monitoring systems and to reduce the discharge of five heavy metals and metalloids (Hg, Cd, As, Cr, Pb) in key regions (East and Central China) by 15% by 2015 from the 2007 base and to control the discharge in nonkey regions below the 2007 level. The second program aims to reduce the number of heavy-metal polluting enterprises and the amount of heavy metal emissions in the Xiangjiang river basin by 50% in 2015 compared to the 2008 levels.52 Assessments on the progress in both programs are keenly awaited. Reducing Metal Phytoavailability. Phytoavailability, rather the total concentration, is the focus of risk management regarding soil contamination with metals, and there are a number of ways to manipulate metal phytoavailability. Liming

Figure 2. Model prediction for grain Cd concentration of Indica and Japonica rice as a function of soil pH and total Cd concentration (converted from 0.43 N HNO3 extractable Cd by a factor of 1.56). Soil CEC was fixed at 10 cmol kg−1. Data are from ref 56.

model prediction corroborates anecdotal evidence that exceedance of the grain Cd limit occurs on some “uncontaminated” soils, most likely due to acidic pH. Upon flooding in paddy systems, the soil pH increases to the neutral range, thus limiting Cd phytoavailability in the soil. However, water is normally drained during the late tillering stage to control infertile tillers and also during the grain filling stages to facilitate harvesting. Rain-fed paddy fields may also be subjected to drought periods. Soil pH drops and Cd phytoavailability increases when the water is drained away, resulting in a massive increase in Cd uptake by rice plants.58 Formation of cadmium sulfide under anaerobic conditions renders Cd less phytoavailable, but oxidation of cadmium sulfide upon water draining is also rapid.59,60 In addition, Mn2+ accumulated in soil solution under flooded conditions, which can inhibit Cd uptake by rice roots via the OsNRAMP5 transporter.61 Under aerobic conditions, soluble Mn2+ is oxidized, thus removing an important inhibitor of Cd uptake. It is well-known that growing rice under flooded conditions can reduce excessive Cd accumulation.62,63 However, this is not always possible, due to the reasons described above. Moreover, continuous flooding can markedly increase As accumulation in rice.64,65 Third, rice cultivars vary widely in the ability to accumulate Cd in the grain and some of the Indica cultivars grown in southern China happen to be Cd accumulators. In general Indica cultivars tend to accumulate more Cd in the grain than Japonica cultivars that are adapted to the temperate region, although within each type there is substantial variation.56,66,67 754

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growth and other agronomic characteristics were unaffected. Furthermore, the mutated gene can be introduced to locally adapted rice cultivars through marker-assisted breeding.94 As OsNRAMP5 is essential for the uptake of Mn,61,91 it remains to be tested if the mutants can acquire sufficient amounts of Mn under low Mn supply conditions (e.g., when paddy soils are drained) without yield losses. Another gene that plays a crucial role in controlling Cd distribution to the above-ground tissues is OsHMA3 through its role in transporting Cd into the vacuoles in the root cells.92 Some rice cultivars possess a nonfunctional allele of OsHMA3, resulting in a much greater translocation of Cd from roots to shoots. Overexpression of a functional allele of OsHMA3 markedly reduced Cd accumulation in rice grain when plants were grown in a contaminated soil without affecting the homeostasis of essential micronutrients.92 Transgenic rice overexpressing a plant gene that can greatly reduce Cd accumulation in the grain should offer real benefit to local residents in the vast area of Cdcontaminated paddy soils in southern China. Such genetically modified cultivars may be more easily acceptable to the consumers. Managing Paddy Water. Where soils are contaminated with Cd or Cd phytoavailability is high due to acidic pH, paddy fields should be maintained under flooded conditions for as long as possible, especially during the grain filling period. However, this practice will inevitably increase As phytoavailability and accumulation in rice.63,65,95 The trade-off between Cd and As accumulation should be considered carefully, according to the degree of the contamination of these two elements. Fertilizer Management. Applications of silicon fertilizers can increase rice grain yield and decrease accumulation of As and Cd.64,96,97 Where soil is deficient in Zn, it is also possible to decrease Cd accumulation in wheat and vegetables by the use of Zn fertilizers.77,98 Changing Cropping Systems. Growing nonfood crops on contaminated soils represents a sensible option. Examples of nonfood crops include cotton, flax, flowers, ornamental plants, and bioenergy crops. However, the change should be implemented only on the more heavily contaminated soils so as not to bring a significant adverse impact on regional grain production and national food security, which is a top priority of the Chinese government. Phytoremediation. Phytoremediation has been touted as a low-cost and environmentally friendly technology to clean up contaminated soils. An advantage of this approach is that the contaminants are removed from the soil for good. For such technologies to be applicable to large areas of contaminated agricultural soils in China, they have to be highly efficient and low cost because farmers cannot afford expensive investment nor to stop farming for years. Phytoextraction of Cd from paddy soils possibly represents the most feasible case among all heavy metals/metalloids because of its relatively low absolute concentrations and high mobility in soils. Phytoextraction of Cd with the Cd/Zn hyperaccumulators Sedum alf redii, Sedum plumbizincicola or high Cd accumulating rice cultivars has been tested in greenhouse or small scale field trials.58,99,100 Whether these technologies can be used in large scale remediation depends on the economics. Concluding Remarks. Soil contamination by heavy metals or metalloids represents a serious problem in China. The issue is both sensitive to the government and a concern to the public. Here we have attempted to evaluate the problem objectively

of acidic soils should be implemented especially in the areas with a high risk of contaminant (e.g., Cd, Pb) exceedance. Various liming materials are available differing in their acid neutralizing capacity, the reaction rate and the cost. To avoid potential injury to crops from the use of a large dose of lime, it may require several dressings of liming materials over a number of cropping seasons to reach the target soil pH (around 6.5). Applications of biochar can also decrease grain Cd and Pb accumulation mainly through its pH effect.73,74 The amount of biochar required to achieve these effects is large (20−40 t ha−1), thus raising the issue of cost and the availability of the materials. Other materials that have been shown to have an immobilizing effect on heavy metals in soil include sepiolite, sewage sludge biochar, red mud and oilseed rape residues.75−77 The efficacies and durability of these immobilizing materials should be tested in field experiments under different conditions. Also, the concentrations of contaminants (e.g., Cd) in liming or other immobilizing materials should be monitored to ensure that these materials do not add significant amounts of contaminants to the soil. Breeding Crop Cultivars with Low Accumulation. A recent field study with a set of 1763 rice accessions of diverse geographic and genetic origin showed a 41- and 154-fold variation in grain Cd concentration under flooded and nonflooded conditions, respectively.78 For grain As the corresponding variation was 12- and 125-fold. Other studies have similarly identified large and heritable genetic differences in grain Cd concentration in a number of staple crops.79 Such large genetic variations could be better exploited to minimize the transfer of toxic metals and metalloids to the food chain. Initially, existing cultivars that are commonly grown can be screened to identify both high and low accumulating cultivars, with the aim of replacing the high with the low accumulating cultivars in the areas having a high risk of metal contamination. In the medium to long-term, low accumulation of toxic metals should become a goal of crop breeding, especially for staple crops such as rice. This involves identification of germplasms possessing low metal accumulation traits, identification of the quantitative trait loci (QTLs) and the associated molecular markers controlling toxic metal accumulation, introgression and pyramiding of the desirable traits into high-yielding and locally adapted cultivars using marker-assisted breeding technologies. Cultivar screening and breeding programs for low metal accumulation are initially quite expensive, but the cost will decline as more breeding lines with the low-metal trait are generated and utilized in new crosses in the breeding program.79 A number of QTLs controlling Cd accumulation in rice66,80−86 (Supporting Information Table S1), wheat,87 soybean,88 and radish89 have been reported. Similarly, QTLs for grain As concentration in rice have been reported (Supporting Information Table S1). Low Cd cultivars of durum wheat have already been registered.90 Recently, a number of genes responsible for Cd uptake into root cells, sequestration of Cd in the vacuoles and Cd distribution to the grain have been identified in rice.91−93 Among these, OsNRAMP5, encoding a Mn/Cd transporter on the plasma membranes of root cells, and OsHMA3, encoding a tonoplast Cd transporter for Cd sequestration in the root vacuoles, hold great promise. Mutation of OsNRAMP5 by ion-beam irradiation resulted in >95% decrease in grain Cd concentration when grown in contaminated paddy soils.94 Grain Cd concentrations in the mutants were found to be nearly undetectable while 755

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Environmental Science & Technology

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and where possible, place it in the international context. It can be argued that the current level and extent of contamination in terms of total concentrations are no worse than other developed countries, but the rates of heavy metal accumulation during the recent decades are apparently greater in China than elsewhere and should be reduced as much as possible. More problematically, the phytoavailability of toxic metals such as Cd and Pb appears to be elevated in some areas of southern China due to the acidic nature of the soil and the cultivation of crop species or cultivars with high accumulation ability, thus posing a serious threat to food safety. A number of mitigation strategies are proposed with the aim to reduce the transfer of toxic metals to the food chain. Shortterm measures include planting low-accumulating cultivars, appropriate irrigation and water management methods, and the use of fertilizers that suppress metal accumulation in crops. Longer term measures include identification of contamination sources and minimization of metal inputs, reducing metal bioavailability with liming or immobilizing materials, breeding of crop cultivars with metal low accumulation, changing cropping system and phytoremediation. Several methods can be used simultaneously to achieve greater effectiveness. On the basis of these principles, a mitigation program incorporating rice variety, irrigation and soil pH amelioration is being piloted in the Xiangjiang river basis by the local government.

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ASSOCIATED CONTENT

S Supporting Information *

Quantitative trait loci (QTLs) for grain Cd and As concentrations in rice. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected] Phone: +86 25 84396509 Fax: +86 25 84399551. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The study was funded by the Natural Science Foundation of China (grant no. 41330853), the special fund for agro-scientific research in the public interest (grant no. 201403015), the special fund for environmental research in the public interest (grant no. 201409041), the Innovative Research Team Development Plan of the Ministry of Education of China (grant no. IRT1256), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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REFERENCES

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