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Policy Analysis

Soil Contamination in China: Current Status and Mitigation Strategies Fang-Jie Zhao, Yibing Ma, Yong-Guan Zhu, Zhong Tang, and Steve P McGrath Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/es5047099 • Publication Date (Web): 16 Dec 2014 Downloaded from http://pubs.acs.org on December 22, 2014

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Policy analysis

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Soil Contamination in China: Current Status and Mitigation Strategies

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Fang-Jie Zhao1, 2*, Yibing Ma3, Yong-Guan Zhu4, Zhong Tang1, Steve P. McGrath2

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Center for Solid Organic Waste Resource Utilization, College of Resources and

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Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China

Jiangsu Key Laboratory for Organic Waste Utilization, Jiangsu Collaborative Innovation

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Hertfordshire AL5 2JQ, U.K.

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Agricultural Sciences, Beijing 100081, China

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Chinese Academy of Sciences, Xiamen 361021, China.

Sustainable Soil and Grassland Systems Department, Rothamsted Research, Harpenden,

Institute of Agricultural Resources and Regional Planning, Chinese Academy of

Key Laboratory of Urban Environment and Health, Institute of Urban Environment,

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* Author for correspondence

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Email: [email protected]

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Phone: +86 25 84396509

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Fax: +86 25 84399551

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ABSTRACT

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China faces great challenges in protecting its soil from contamination caused by rapid

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industrialization and urbanization over the last three decades. Recent nationwide surveys

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show that 16% of the soil samples, 19% for the agricultural soils, are contaminated based on

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China’s soil environmental quality limits, mainly with heavy metals and metalloids.

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Comparisons with other regions of the world show that the current status of soil

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contamination, based on the total contaminant concentrations, is not worse in China.

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However, the concentrations of some heavy metals in Chinese soils appear to be increasing at

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much greater rates. Exceedance of the contaminant limits in food crops is widespread in some

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areas, especially southern China, due to elevated inputs of contaminants, acidic nature of the

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soil and crop species or cultivars prone to heavy metal accumulation. Minimizing the

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transfer of contaminants from soil to the food chain is a top priority. A number of options are

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proposed, including identification of the sources of contaminants to agricultural systems,

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minimization of contaminant inputs, reduction of heavy metal phytoavailability in soil with

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liming or other immobilizing materials, selection and breeding of low accumulating crop

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cultivars, adoption of appropriate water and fertilizer management, bioremediation, and

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change of land use to grow non-food crops. Implementation of these strategies requires not

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only technological advances, but also social-economic evaluation and effective enforcement

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of environmental protection law.

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Introduction The status of soil contamination in China has attracted much public attention both

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domestically and internationally. The public concern arises largely from the scare about the

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safety of agricultural produce. Recently, the Ministry of Environmental Protection (MEP)

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and the Ministry of Land and Resources (MLR) of the People’s Republic of China issued a

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joint report on the current status of soil contamination in China 1. The report presents an

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overall grim situation with regard to the environmental quality of China’s soils. According to

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the report, soils in some areas, especially those surrounding mining and industry activities,

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have been seriously contaminated, whilst the quality of farmland soil is also of particular

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concern. The report is based on extensive surveys of soils conducted between 2005 and 2013,

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covering more than 70% of China’s land area. Surface (0-20 cm) soil samples were collected

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from 8 × 8 km grids and analyzed for 13 inorganic contaminants (arsenic, cadmium, cobalt,

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chromium, copper, fluoride, mercury, manganese, nickel, lead, selenium, vanadium, zinc)

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and 3 types of organic contaminants (hexachlorocyclohexane,

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dichlorodiphenyltrichloroethane and polyaromatic hydrocarbons). Of all the samples

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analyzed, 16.1% exceed the environmental quality standard set by the MEP; for agricultural

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soils the percentage of exceedance is even greater at 19.4% (equivalent to approximately 26

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million ha assuming that that the area is proportional to the number of survey samples).

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Contamination by heavy metals and metalloids (here, referring to the 8 elements listed in

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Table 1) accounts for the majority (82.4%) of the soils classified as being contaminated, with

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organic contaminants accounting for the rest. Among the heavy metals and metalloids,

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cadmium (Cd) ranks the first in the percentage of soil samples (7.0%) exceeding the MEP

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limit.

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Arable land per capita in China is less than half of the world average, so protecting

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this precious resource from degradation and contamination has now been placed very high in

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the government’s agenda 2. Large sums of public funding have also been promised for the

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remediation of contaminated soils 3. However, how this should be done has been a subject of

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intense debate. Here, we present an appraisal of China’s current status of soil contamination

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and the effect on food safety, and propose strategies to deal with this worsening problem. The

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focus of this policy analysis is on heavy metals and metalloids in agricultural soils, as these

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can present a serious threat to human health through the food chain. Special emphasis is

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placed on Cd, as it is the most critical toxic metal threatening food safety and agricultural

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sustainability in China.

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Soil quality standards in China

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Because heavy metals and metalloids in soils are derived from both natural and

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anthropogenic sources, it is not straight forward to determine if a soil is contaminated. In the

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recent MEP/MLR soil contamination survey, the status of soil contamination was determined

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by comparing the total concentration of a contaminant to the benchmark values of the

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Chinese environmental quality standard for soils issued by the MEP in 1995. The standard

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specifies three classes of benchmark values for eight heavy metals or metalloids and two

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pesticides 4 (Table 1). Class I values are considered to represent the natural background, to be

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used in the protection of regional natural ecosystems from contamination. Class II is set up to

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protect agricultural production and human health via the food chain, and can be applied to

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agricultural, orchard and pasture land. The class II values are dependent on soil pH and land

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use. In the recent MEP and MLR soil contamination survey, a soil is considered to be

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contaminated if a heavy metal or metalloid is above the class II value; the degree of

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contamination is designated as light, medium or severe when the concentration is 1 – 3, 3 – 5

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or >5 times the benchmark value, respectively. Class III is for the protection of crops or

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forests from phytotoxicity and may also be used where the natural background is elevated.

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A number of issues have been raised with regard to the China’s soil quality standards.

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First, for a country as large and geochemically diverse as China, natural background

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concentrations of heavy metals and metalloids are not single values but are likely to vary

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substantially across the country. Natural background levels depend on the soil parent

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materials and pedogenetic processes, and therefore vary among different soil types 5-8. For

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example, soils developed from serpentine rocks are naturally enriched with nickel and

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chromium. The concentrations of several heavy metals are known to correlate closely with

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those of iron or aluminum oxides in soils, reflecting the parallel influences of pedogensis on

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these elements 5, 9. A pan-European comparison revealed higher background levels of several

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heavy metals and metalloids in the more weathered soils of southern Europe than in the

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younger soils of northern Europe, with the break in concentrations coinciding with the

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maximum extent of the last glaciation 10. A national soil survey conducted in the early 1980s

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showed that the 90th percentile Cd concentrations in both the A and C soil horizons were

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markedly higher in Guizhou and Guangxi provinces in southwest China than in the other 5

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regions of China 11. Furthermore, soils developed from sedimentary parent materials,

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particularly sedimentary limestone, tend to have higher Cd concentrations than others 11. In

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the MEP/MLR soil contamination survey, soils with a high natural background of heavy

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metals or metalloids would also be classified as “contaminated”.

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Second, there are debates on whether the Class II values are over-protective or under-

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protective. Recent studies using soil to plant transfer models suggest that the Class II Cd limit

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may be set too low (i.e. over-protective) for soils with near neutral to alkaline pH 12, 13.

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Certainly, the 0.3 – 0.6 mg kg-1 soil Cd limit (Table 1) is lower than either the 1 – 3 mg kg-1

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limit adopted by the EU for land applications of sewage sludge or up to 39 mg kg-1 in the US-

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EPA’s rules on land applications of biosolids 14. The EU risk assessment on Cd has derived

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the predicted no effect concentrations (PNECs) of 0.6 – 2.3 mg kg-1 for the protection of

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human health, mammals and bird, plants and soil organisms 15, whilst the US-EPA

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recommends a screening value (ECOSSL) of 0.4 – 0.8 mg kg-1, above which further

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investigations are needed to determine if a site might be hazardous 16 . In highly acidic soils,

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however, food Cd limits may be exceeded even when soil Cd concentrations are below 0.3

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mg kg-1 13. On the other hand, there is some evidence that the Class II Pb limits may be set

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too high and may lead to non-compliance with the food Pb limits 17. The exposure pathway of

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soil ingestion by humans is also not considered in setting the Pb limits.

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Clearly, both issues would need to be addressed in any future revision of the soil

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quality standards in China, taking into account evidence accumulated since the standard was

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issued in 1995. When assessing the current status of soil contamination in China, it is

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important to bear in mind the assessment is relative to the magnitude of the benchmark values

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in the soil quality standard and some of the “contaminated” soils are due to naturally high

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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

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contaminated with Cd (7%) is because of the low Class II values: 0.3 and 0.6 mg kg-1 for

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soils with pH 7.5, respectively (Table 1). Other countries may have higher Cd

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concentrations in their soils, compared with the recent soil survey results in China. For

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example, a national soil inventory shows that 45% and 20% of the soils in England and 6

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Wales exceed 0.3 and 0.6 mg kg-1, respectively 18. In continental Europe, the 75th percentile

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value of soil Cd was found to be 0.27 and 0.32 mg kg-1 for soils from agricultural and grazing

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land, respectively 10, which means that a considerable proportion of European soils is over

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0.3 mg kg-1 limit. In the US, the 75th percentile for agricultural areas was 0.34 mg kg-1 19.

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These comparisons help to place the current status of soil contamination in China in a

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different perspective: in terms of the total concentrations it is not worse than other regions

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such as Europe and the US. In the case of Ni, the relatively high percentage of contamination

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in China (4.8%, Table 1) is also due to, at least partly, the Class II values being set close to

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the Class I (natural background) level. On the other hand, the relatively low percentages of

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soil samples identified as being contaminated with Pb or Cr (Table 1) can be attributed to the

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large Class II values in the soil quality standard.

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Whilst the current status of soil contamination in China may not be as grim as

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perceived in popular media, there are reasons for concern. This is because large quantities of

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heavy metals and metalloids have been discharged into the environment over the last three

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decades coinciding with rapid industrialization and urbanization in China. In 2012, 22 billion

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tons of waste water, 64 trillion cubic meters of waste gas and 3.3 billion tons of solid waste

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were discharged from industrial sources in China 20. The total amount of five heavy metals

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and metalloids (Hg, Cd, Cr, Pb and As) discharged in industrial waste water reached 441 tons

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in 2012, although the discharge has been decreasing during recent years (Fig. 1). The

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amounts of heavy metals released from mining are not quantified, but are probably

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substantially higher. In 2010, China consumed 3.38 billion tons of coal 21, which is likely to

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emit approximately 9000, 360, 450 and 25000 tons of As, Cd, Hg and Pb, respectively, based

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on the average concentrations of these metals in coal and their emission factors 22. China is

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also the largest producer and consumer of many heavy metals in the world. For example,

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China produces and consumes about a third of the refinery cadmium in the world, most of it

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being used in the production of nickel-cadmium batteries 23. Uncontrolled discharges of

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waste water, gas and solids have cumulatively raised the burden of heavy metals in the

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environment. A comparison between nationwide soil surveys conducted recently and those in

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the late 1980s shows clear increases in the total concentrations of a number of heavy metals

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and metalloids during the 25-year period. For example, average soil Cd concentrations

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increased by 10 – 40% in the western and northern China and by over 50% in the coastal

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region and the southwest of the country 24. Based on the inventory of inputs and outputs in

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agricultural systems not subjected to serious contaminations from point-sources, Luo et al. 22 7

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estimated that the Cd concentration in Chinese agricultural soils has been increasing at an

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average rate of 0.004 mg Cd kg-1 year-1. This is much greater than those reported elsewhere,

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e.g. 0.00033 mg Cd kg-1 year-1 in Europe 25, and would lead to a doubling of the average soil

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Cd concentration in China in 50 years if the input/output trend continued. Clearly, such an

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increase rate is worrying and must be reduced as soon and as much as possible. For

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comparison, it would take between 364 and 2433 years for the average concentrations of

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other heavy metals or metalloids in soil to increase from their background levels to the Class

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II limits 22. Therefore, Cd stands out as the most critical heavy metal for agricultural soils in

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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

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through the food chain 25, keeping the metal concentrations in the edible parts of agricultural

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crops in check is an important and urgent task in China. An apparent paradox emerges when

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the soil-crop data in China and the UK are compared. Whilst soil Cd concentrations in the

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UK are generally higher than those in China, wheat grain produced in the UK rarely exceeds

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the 0.2 mg Cd kg-1 limit of EU and FAO/WHO; exceedance was found in less than 0.2% of

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survey samples analyzed 26, 27. In contrast, rice, the most important crop grown in southern

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China, appears to be problematic in meeting the 0.2 mg Cd kg-1 limit of the Chinese food

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standard. In some areas of southern China, particularly those impacted by mining and

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industrial activities, considerable proportions of rice grain exceed the Cd limit 28, causing

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widespread public concern in recent years. A recent survey of rice grain from a county

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located in the Xiangjiang river basin in Hunan province, one of the most important rice

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growing areas in China, showed that 60% of the samples exceed the 0.2 mg Cd kg-1 limit, and

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11% contain >1.0 mg Cd kg-1 29. On a countrywide scale, market basket surveys reported

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between 2 and 13% of rice grain samples exceeding the limit 30-32.

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China has adopted a food standard limit of 0.2 mg Cd kg-1, which is stricter than the

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FAO/WHO’s limit of 0.4 mg kg-1 for rice 33. This strict limit is deemed necessary because of

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the high consumption of rice by Chinese population: 238 and 327 g day-1 for national average

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and southern population average, respectively 34. Cd intake from rice alone with a Cd

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concentration of 0.2 mg kg-1 would amount to 0.73 and 1.01 µg kg-1 body weight day-1 for the 8

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national average (for adults of 65 kg body weight); the latter already exceeds the FAO/WHO

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tolerable daily intake (TDI) of 0.83 µg kg-1 body weight day-1 35. For populations based on a

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subsistence rice diet, Cd in rice may pose a greater risk to humans because of the generally

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low concentrations of Fe and Zn in the diet, which could result in greater uptake of Cd 36, and

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such populations typically consume large amounts of rice (~500 g day-1). Moreover, residents

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living in contaminated areas who consume mainly locally produced grain and vegetables are

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particularly vulnerable. A number of studies have shown that the dietary Cd intake for

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residents in some mining impacted areas in China is well over the TDI level, with rice being

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the most important source 37-40. In some cases the daily Cd intake exceeds 300 µg day-1 (4.6

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µg kg-1 body weight day-1), which is likely to cause severe chronic Cd poisoning 41. There is

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also strong evidence linking elevated exposure to Cd with renal dysfunction and osteoporosis,

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and increased cancer mortality rate in populations impacted by mining activities in China 38,

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42-47

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. Apart from Cd, accumulation of As and Pb in rice is also of concern. A survey of rice

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grain collected from mining-impacted paddy fields in Hunan province showed that 65, 50,

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and 34% of the samples fail the national food standards for Cd, As, and Pb, respectively 28, 48.

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Rice grain produced in a Hg mining and smelting area in Guizhou, southwest China, also

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contains significant amounts of methylmercury, a highly toxic species of Hg 49.

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Approximately a third of the local farmers in the area had a methylmercury intake exceeding

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the reference dose of 0.1 µg kg-1 bw day-1 established by the U.S. Environmental Protection

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Agency, with rice contributing to 95% of the intake 50.

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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

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than in other regions for a number of reasons. First, mining of base metals and metal smelting

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have been important economic activities in some parts of southern China for a long time.

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These activities have released large quantities of heavy metals and metalloids into the

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environment due to inadequate enforcement of environmental protection law. Taking Hunan

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province (the largest rice producing province in China) as an example, it has been estimated

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that mining, smelting and other industries released 610, 31, 136 and 4 tons year-1 of Pb, Cd,

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Cr and Hg, respectively, into the Xiangjiang river, a major tributary of the Yangtze River 51. 9

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Xiangjiang river basin is an important rice producing area, but is also among the most

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contaminated areas in China 52. Some stream water in the Xiangjiang River catchment area

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contains as much as 40 µg Cd L-1, 8 times the drinking water limit 29, whilst Liu et al. 51

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reported maximum concentrations of 430 µg Cd L-1, 500 µg As L-1 and 138 µg Pb L-1 in

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some sections of Xiangjiang river. As the double-rice cropping system, a typical cropping

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system in southern China, consumes large quantities irrigation water, inputs of heavy metals

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into the soil can be substantial. Assuming 1 m irrigation water per year, the input of Cd into

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the paddy system would amount to 50, 100 and 400 g ha-1, respectively, with Cd

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concentrations in water of 5, 10 and 40 µg L-1 (these concentrations correspond to the

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drinking water limit, irrigation water limit and the highest concentration reported by Du et

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al.29, respectively). These inputs could raise the Cd concentration in the topsoil (0-20 cm) by

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0.02, 0.04 and 0.15 mg kg-1, respectively, in a single year if there were no losses of Cd from

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the system. Based on the typical biomass (12 tons ha-1 for grain and straw, respectively, for

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early and late rice) and the range of Cd concentrations in rice grain (0.05 – 0.5 mg kg-1) and

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straw (0.4 – 4 mg kg-1) in southern China, crop uptake is likely to remove 5 – 55 g ha-1of Cd

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from the soil depending on the status of Cd contamination in the paddy field (Table 2), i.e.

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only about one tenth of the Cd inputs from irrigation water. There are other sources of heavy

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metals and metalloids, such as atmospheric deposition, fertilizers and manures (Table 2). Due

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to metal smelting and coal combustion, the rates of atmospheric deposition in China are

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higher than those in developed countries 22. Atmospheric deposition of Cd ranges from 0.4 to

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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

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current mean of EU of 0.35 g ha-1 yr-1 53. Phosphate fertilizers can contain considerable

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amounts of Cd. But fortunately, many rock phosphates in China have low levels of Cd and

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consequently, home-produced phosphate fertilizers are not an important source of Cd to

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agricultural soils, although some imported phosphate fertilizers used to make compound

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fertilizers may be elevated in Cd 22, 54. Some organic manures contain high levels of heavy

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metals or metalloids, especially Zn, Cu, As and occasionally, Cd 22. Where sewage sludge is

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applied onto agricultural land, it could also add significant amounts of heavy metals,

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especially Zn and Cu 22. The data for losses of heavy metals through runoff and leaching are

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scarce, making mass balance calculations difficult. However, it is apparent from Table 2 that

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irrigation is the dominant source of Cd in the double rice cropping system in southern China

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if the water used contains elevated levels of Cd.

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The second important reason causing high accumulation of cationic heavy metals in

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rice and vegetables is the acidic nature of the soils in many areas of southern China, leading

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to a high phytoavailability of Cd in the soil. In the tropical and subtropical regions of

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southern China, red soil and the paddy soil developed from this soil type are inherently acidic.

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Use of acidifying nitrogen fertilizers, crop uptake of base cations and acid deposition from

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the atmosphere have contributed to significant soil acidification in major croplands in China

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over the last three decades 55. Approximately half of the paddy soils in Hunan province have

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a pH lower than 5.5. Several field or pot studies have shown that paddy soil pH has a highly

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significant effect on the accumulation Cd in rice grain 13, 56, 57. Based on the regression model

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presented by Romkens et al. 56, it can be predicted that for Indica rice cultivars which are

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commonly grown in southern China, grain Cd may exceed the 0.2 mg kg-1 limit when soil Cd

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concentration is above 0.18 and 0.9 mg kg-1 at soil pHs of 5 and 7, respectively (Fig. 2). This

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model prediction corroborates anecdotal evidence that exceedance of the grain Cd limit

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occurs on some “uncontaminated” soils, most likely due to acidic pH. Upon flooding in

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paddy systems, the soil pH increases to the neutral range, thus limiting Cd phytoavailability

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in the soil. However, water is normally drained during the late tillering stage to control

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infertile tillers and also during the grain filling stages to facilitate harvesting. Rain-fed paddy

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fields may also be subjected to drought periods. Soil pH drops and Cd phytoavailability

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increases when the water is drained away, resulting in a massive increase in Cd uptake by

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rice plants 58. Formation of cadmium sulfide under anaerobic conditions renders Cd less

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phytoavailable, but oxidation of cadmium sulfide upon water draining is also rapid 59, 60. In

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addition, Mn2+ accumulated in soil solution under flooded conditions, which can inhibit Cd

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uptake by rice roots via the OsNRAMP5 transporter 61. Under aerobic conditions, soluble

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Mn2+ is oxidized, thus removing an important inhibitor of Cd uptake. It is well known that

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growing rice under flooded conditions can reduce excessive Cd accumulation 62, 63. However,

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this is not always possible, due to the reasons described above. Moreover, continuous

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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

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of the Indica cultivars grown in southern China happen to be Cd accumulators. In general

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Indica cultivars tend to accumulate more Cd in the grain than Japonica cultivars that are

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adapted to the temperate region, although within each type there is substantial variation 56, 66,

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clear that Indica rice is more likely to exceed the grain Cd limit than Japonica rice; for the

. Based on the regression models developed for the average Indica and Japonica rice 56, it is 11

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latter exceedance is predicted with a soil total Cd of 0.55 and 1.7 mg kg-1 at pH 5 and 7,

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respectively (Fig. 2). On acidic soils, some vegetables, such as carrot, leafy, brassica and

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solanaceous vegetables, are also prone to Cd accumulation 13, 68-70, therefore adding to the

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dietary Cd intake of the local residents 70-72.

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So, the combination of soil contamination, high phytoavailability in acidic soils and

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cultivation of heavy metal accumulating rice cultivars and vegetable species substantially

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increases the risk of the transfer of heavy metals from soil to the food chain in southern China.

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Under these conditions, naturally elevated concentrations of heavy metals may pose a risk

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similar to those from anthropogenic activities. The last two factors discussed above probably

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also explain why such risk is higher in southern China than in Europe at the same level of

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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

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metalloid contamination in food crops in China, some of which are discussed below.

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Implementation of various strategies requires not only technological advances, but also

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social-economic evaluation and effective enforcement of environmental protection law, as

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well as government subsidy.

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Identify and stop the sources of contamination. The first step to combat heavy metal

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contamination in the soil-plant systems is to identify and stop the main sources of

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contamination. This requires more stringent monitoring and effective enforcement of

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environmental protection law, especially with regard to large emission sources such as

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mining, smelting and other metal consuming industries. There is an urgent need to establish

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national and regional inventories of metal and metalloid concentrations in water used for

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irrigation and of atmospheric inputs. This would enable realistic appraisal of the current

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contamination status and prediction of the future trend. Where irrigation water contains

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elevated levels of metals or metalloids, simple and effective techniques should be developed

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to remove the contaminants before water reaches the field; where this is not possible,

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alternative clean water sources would need to be found. Starting in 2011, the Chinese

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government has initiated two large national programs to combat heavy metal pollution: the

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12th five-year plan for preventing heavy metal pollution and the Xiangjiang river basin 12

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control plan for heavy metal pollution, each with funding of tens of billions of Chinese Yuan

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discharge of five heavy metals and metalloids (Hg, Cd, As, Cr, Pb) in key regions (East and

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Central China) by 15% by 2015 from the 2007 base and to control the discharge in non-key

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regions below the 2007 level. The second program aims to reduce the number of heavy-metal

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polluting enterprises and the amount of heavy metal emissions in the Xiangjiang river basin

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by 50% in 2015 compared to the 2008 levels 52. Assessments on the progress in both

334

programs are keenly awaited.

335

Reducing metal phytoavailability. Phytoavailability, rather the total concentration, is the

336

focus of risk management regarding soil contamination with metals, and there are a number

337

of ways to manipulate metal phytoavailability. Liming of acidic soils should be implemented

338

especially in the areas with a high risk of contaminant (e.g. Cd, Pb) exceedance. Various

339

liming materials are available differing in their acid neutralizing capacity, the reaction rate

340

and the cost. To avoid potential injury to crops from the use of a large dose of lime, it may

341

require several dressings of liming materials over a number of cropping seasons to reach the

342

target soil pH (around 6.5). Applications of biochar can also decrease grain Cd and Pb

343

accumulation mainly through its pH effect 73, 74. The amount of biochar required to achieve

344

these effects is large (20 – 40 t ha-1), thus raising the issue of cost and the availability of the

345

materials. Other materials that have been shown to have an immobilizing effect on heavy

346

metals in soil include sepiolite, sewage sludge biochar, red mud and oilseed rape residues 75-77.

347

The efficacies and durability of these immobilizing materials should be tested in field

348

experiments under different conditions. Also, the concentrations of contaminants (e.g. Cd) in

349

liming or other immobilizing materials should be monitored to ensure that these materials do

350

not add significant amounts of contaminants to the soil.

351

Breeding crop cultivars with low accumulation. A recent field study with a set of 1763 rice

352

accessions of diverse geographic and genetic origin showed a 41- and 154-fold variation in

353

grain Cd concentration under flooded and non-flooded conditions, respectively 78. For grain

354

As the corresponding variation was 12- and 125-fold. Other studies have similarly identified

355

large and heritable genetic differences in grain Cd concentration in a number of staple crops

356

79

357

metals and metalloids to the food chain. Initially, existing cultivars that are commonly grown

358

can be screened to identify both high and low accumulating cultivars, with the aim of

. The first program aims to strengthen the control and monitoring systems and to reduce the

. Such large genetic variations could be better exploited to minimize the transfer of toxic

13

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replacing the high with the low accumulating cultivars in the areas having a high risk of metal

360

contamination. In the medium to long term, low accumulation of toxic metals should become

361

a goal of crop breeding, especially for staple crops such as rice. This involves identification

362

of germplasms possessing low metal accumulation traits, identification of the quantitative

363

trait loci (QTLs) and the associated molecular markers controlling toxic metal accumulation,

364

introgression and pyramiding of the desirable traits into high-yielding and locally adapted

365

cultivars using marker-assisted breeding technologies. Cultivar screening and breeding

366

programs for low metal accumulation are initially quite expensive, but the cost will decline as

367

more breeding lines with the low-metal trait are generated and utilized in new crosses in the

368

breeding program 79.

369

A number of QTLs controlling Cd accumulation in rice 66, 80-86 (Supporting

370

information Table S1), wheat 87, soybean 88 and radish 89 have been reported. Similarly,

371

QTLs for grain As concentration in rice have been reported (Supporting information Table

372

S1). Low Cd cultivars of durum wheat have already been registered 90. Recently, a number of

373

genes responsible for Cd uptake into root cells, sequestration of Cd in the vacuoles and Cd

374

distribution to the grain have been identified in rice 91-93. Amongst these is OsNRAMP5,

375

encoding a Mn/Cd transporter on the plasma membranes of root cells, and OsHMA3,

376

encoding a tonoplast Cd transporter for Cd sequestration in the root vacuoles, hold great

377

promise. Mutation of OsNRAMP5 by ion-beam irradiation resulted in >95% decrease in grain

378

Cd concentration when grown in contaminated paddy soils 94. Grain Cd concentrations in the

379

mutants were found to be nearly undetectable whilst growth and other agronomic

380

characteristics were unaffected. Furthermore, the mutated gene can be introduced to locally

381

adapted rice cultivars through marker-assisted breeding 94. As OsNRAMP5 is essential for

382

the uptake of Mn 61, 91, it remains to be tested if the mutants can acquire sufficient amounts of

383

Mn under low Mn supply conditions (e.g. when paddy soils are drained) without yield losses.

384

Another gene that plays a crucial role in controlling Cd distribution to the above-ground

385

tissues is OsHMA3 through its role in transporting Cd into the vacuoles in the root cells 92.

386

Some rice cultivars possess a non-functional allele of OsHMA3, resulting in a much greater

387

translocation of Cd from roots to shoots. Over-expression of a functional allele of OsHMA3

388

markedly reduced Cd accumulation in rice grain when plants were grown in a contaminated

389

soil without affecting the homeostasis of essential micronutrients 92. Transgenic rice

390

overexpressing a plant gene that can greatly reduce Cd accumulation in the grain should offer 14

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real benefit to local residents in the vast area of Cd-contaminated paddy soils in southern

392

China. Such genetically modified cultivars may be more easily acceptable to the consumers.

393

Managing paddy water. Where soils are contaminated with Cd or Cd phytoavailability is

394

high due to acidic pH, paddy fields should be maintained under flooded conditions for as long

395

as possible, especially during the grain filling period. However, this practice will inevitably

396

increase As phytoavailability and accumulation in rice 63, 65, 95. The tradeoff between Cd and

397

As accumulation should be considered carefully, according to the degree of the

398

contamination of these two elements.

399

Fertilizer management.

400

and decrease accumulation of As and Cd 64, 96, 97. Where soil is deficient in Zn, it is also

401

possible to decrease Cd accumulation in wheat and vegetables by the use of Zn fertilizers 77,

402

98

403

Changing cropping systems. Growing non-food crops on contaminated soils represents a

404

sensible option. Examples of non-food crops include cotton, flax, flowers, ornamental plants

405

and bioenergy crops. However, the change should be implemented only on the more heavily

406

contaminated soils so as not to bring a significant adverse impact on regional grain

407

production and national food security, which is a top priority of the Chinese government.

408

Phytoremediation. Phytoremediation has been touted as a low-cost and environmentally

409

friendly technology to clean up contaminated soils. An advantage of this approach is that the

410

contaminants are removed from the soil for good. For such technologies to be applicable to

411

large areas of contaminated agricultural soils in China, they have to be highly efficient and

412

low cost because farmers cannot afford expensive investment nor to stop farming for years.

413

Phytoextraction of Cd from paddy soils possibly represents the most feasible case among all

414

heavy metals/metalloids because of its relatively low absolute concentrations and high

415

mobility in soils. Phytoextraction of Cd with the Cd/Zn hyperaccumulator Sedum alfredii,

416

Sedum plumbizincicola or high Cd accumulating rice cultivars has been tested in greenhouse

417

or small scale field trials 58, 99, 100. Whether these technologies can be used in large scale

418

remediation depends on the economics.

419

Concluding remarks

Applications of silicon fertilizers can increase rice grain yield

.

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Soil contamination by heavy metals or metalloids represents a serious problem in

421

China. The issue is both sensitive to the government and a concern to the public. Here we

422

have attempted to evaluate the problem objectively and where possible, place it in the

423

international context. It can be argued that the current level and extent of contamination in

424

terms of total concentrations are no worse than other developed countries, but the rates of

425

heavy metal accumulation during the recent decades are apparently greater in China than

426

elsewhere and should be reduced as much as possible. More problematically, the

427

phytoavailability of toxic metals such as Cd and Pb appears to be elevated in some areas of

428

southern China due to the acidic nature of the soil and the cultivation of crop species or

429

cultivars with high accumulation ability, thus posing a serious threat to food safety.

430

A number of mitigation strategies are proposed with the aim to reduce the transfer of

431

toxic metals to the food chain. Short-term measures include planting low-accumulating

432

cultivars, appropriate irrigation and water management methods, and the use of fertilizers that

433

suppress metal accumulation in crops. Longer term measures include identification of

434

contamination sources and minimization of metal inputs, reducing metal bioavailability with

435

liming or immobilizing materials, breeding of crop cultivars with metal low accumulation,

436

changing cropping system and phytoremediation. Several methods can be used

437

simultaneously to achieve greater effectiveness. Based on these principles, a mitigation

438

program incorporating rice variety, irrigation and soil pH amelioration is being piloted in the

439

Xiangjiang river basis by the local government.

440 441

ACKNOWLEDGEMENTS

442

The study was funded by the Natural Science Foundation of China (grant No. 41330853), the

443

special fund for agro-scientific research in the public interest (grant No. 201403015), the

444

special fund for environmental research in the public interest (grant No. 201409041), the

445

Innovative Research Team Development Plan of the Ministry of Education of China (grant

446

no. IRT1256) and the Priority Academic Program Development of Jiangsu Higher Education

447

Institutions (PAPD).

448 449

Supporting Information 16

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Quantitative trait loci (QTLs) for grain Cd and As concentrations in rice. This information is

451

available free of charge via the Internet at http://pubs.acs.org/ .”

452 453

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Khan, S.; Reid, B. J.; Li, G.; Zhu, Y. G. Application of biochar to soil reduces cancer

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four metal-contaminated soils using the cadmium/zinc hyperaccumulator Sedum

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753

Table 1. Chinese soil environmental quality standards (total concentration in mg kg-1) and the

754

percentages of soil samples exceeding the Class II standards in the recent national soil

755

contamination survey 1, 4 Metal/metalloid

Class I (natural

Class II pH < 6.5

pH 6.5 ~ 7.5

pH > 7.5

Class III

% exceeding

pH > 6.5

the limit

background) Cd

0.2

0.3

0.3

0.6

1.0

7.0

As: Paddy

15

30

25

20

30

2.7*

Upland

15

40

30

25

40

Hg

0.15

0.3

0.5

1.0

1.5

1.6

Cu: farmland

35

50

100

100

400

2.1*

-

150

200

200

400

Pb

35

250

300

350

500

1.5

Cr: Paddy

90

250

300

350

400

1.1*

90

150

200

250

300

Zn

100

200

250

300

500

0.9

Ni

40

40

50

60

200

4.8

Orchard

Upland

756

* The percentage exceedance is for all soil types.

757

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758

Table 2. Mass balance of Cd in double-rice cropping systems in southern China Cd inputs (g ha-1 yr-1)

759

Page 28 of 31

Cd outputs (g ha-1 yr-1)

Irrigation (1 m water, 0.1 – 40 ppb Cd)

1 – 400

Rice uptake

5 – 55

Phosphate fertilizers

0.04 - 2

Leaching

ND*

Organic manures

0 - 10

Runoff

ND*

Atmospheric deposition (mean)

0.4 – 25 (4)

* ND, no data available.

760

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List of Figures:

762

Figure 1. Discharge of five heavy metals or metalloid in industrial waste water in China 20.

763

Figure 2. Model prediction for grain Cd concentration of Indica and Japonica rice as a

764

function of soil pH and total Cd concentration (converted from 0.43 N HNO3 extractable Cd

765

by a factor of 1.56). Soil CEC was fixed at 10 cmol kg-1. Data are from 56.

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766

1000

Hg

Amount (t/year)

Cd Cr(VI)

100

Pb As 10

1 2005 2006 2007 2008 2009 2010 2011 2012 Year 767 768

Figure 1. Discharge of heavy metals in industrial waste water in China 20.

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769

Grain Cd (mg kg-1)

1.4 1.2 1.0 0.8

Indica rice pH 5 pH 6 pH 7

0.6 0.4 0.2 0.0 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2

Soil Cd (mg kg-1) 770

Grain Cd (mg kg-1)

1.4 1.2 1.0 0.8

Japonica rice pH 5 pH 6 pH 7

0.6 0.4 0.2 0.0 0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2

Soil Cd (mg kg-1) 771 772

Figure 2. Model prediction for grain Cd concentration of Indica and Japonica rice as a

773

function of soil pH and total Cd concentration (converted from 0.43 N HNO3 extractable Cd

774

by a factor of 1.56). Soil CEC was fixed at 10 cmol kg-1. Data are from 56.

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