Subscriber access provided by UNIV OF PITTSBURGH
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
Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a free service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are accessible to all readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.
Page 1 of 31
Environmental Science & Technology
1
Policy analysis
2 3
Soil Contamination in China: Current Status and Mitigation Strategies
4 5
Fang-Jie Zhao1, 2*, Yibing Ma3, Yong-Guan Zhu4, Zhong Tang1, Steve P. McGrath2
6 7
1
8
Center for Solid Organic Waste Resource Utilization, College of Resources and
9
Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China
Jiangsu Key Laboratory for Organic Waste Utilization, Jiangsu Collaborative Innovation
10
2
11
Hertfordshire AL5 2JQ, U.K.
12
3
13
Agricultural Sciences, Beijing 100081, China
14
4
15
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,
16 17
* Author for correspondence
18
Email:
[email protected]
19
Phone: +86 25 84396509
20
Fax: +86 25 84399551
1
ACS Paragon Plus Environment
Environmental Science & Technology
21
ABSTRACT
22
China faces great challenges in protecting its soil from contamination caused by rapid
23
industrialization and urbanization over the last three decades. Recent nationwide surveys
24
show that 16% of the soil samples, 19% for the agricultural soils, are contaminated based on
25
China’s soil environmental quality limits, mainly with heavy metals and metalloids.
26
Comparisons with other regions of the world show that the current status of soil
27
contamination, based on the total contaminant concentrations, is not worse in China.
28
However, the concentrations of some heavy metals in Chinese soils appear to be increasing at
29
much greater rates. Exceedance of the contaminant limits in food crops is widespread in some
30
areas, especially southern China, due to elevated inputs of contaminants, acidic nature of the
31
soil and crop species or cultivars prone to heavy metal accumulation. Minimizing the
32
transfer of contaminants from soil to the food chain is a top priority. A number of options are
33
proposed, including identification of the sources of contaminants to agricultural systems,
34
minimization of contaminant inputs, reduction of heavy metal phytoavailability in soil with
35
liming or other immobilizing materials, selection and breeding of low accumulating crop
36
cultivars, adoption of appropriate water and fertilizer management, bioremediation, and
37
change of land use to grow non-food crops. Implementation of these strategies requires not
38
only technological advances, but also social-economic evaluation and effective enforcement
39
of environmental protection law.
2
ACS Paragon Plus Environment
Page 2 of 31
Page 3 of 31
40
Environmental Science & Technology
TOC art
41
3
ACS Paragon Plus Environment
Environmental Science & Technology
42
Introduction The status of soil contamination in China has attracted much public attention both
43 44
domestically and internationally. The public concern arises largely from the scare about the
45
safety of agricultural produce. Recently, the Ministry of Environmental Protection (MEP)
46
and the Ministry of Land and Resources (MLR) of the People’s Republic of China issued a
47
joint report on the current status of soil contamination in China 1. The report presents an
48
overall grim situation with regard to the environmental quality of China’s soils. According to
49
the report, soils in some areas, especially those surrounding mining and industry activities,
50
have been seriously contaminated, whilst the quality of farmland soil is also of particular
51
concern. The report is based on extensive surveys of soils conducted between 2005 and 2013,
52
covering more than 70% of China’s land area. Surface (0-20 cm) soil samples were collected
53
from 8 × 8 km grids and analyzed for 13 inorganic contaminants (arsenic, cadmium, cobalt,
54
chromium, copper, fluoride, mercury, manganese, nickel, lead, selenium, vanadium, zinc)
55
and 3 types of organic contaminants (hexachlorocyclohexane,
56
dichlorodiphenyltrichloroethane and polyaromatic hydrocarbons). Of all the samples
57
analyzed, 16.1% exceed the environmental quality standard set by the MEP; for agricultural
58
soils the percentage of exceedance is even greater at 19.4% (equivalent to approximately 26
59
million ha assuming that that the area is proportional to the number of survey samples).
60
Contamination by heavy metals and metalloids (here, referring to the 8 elements listed in
61
Table 1) accounts for the majority (82.4%) of the soils classified as being contaminated, with
62
organic contaminants accounting for the rest. Among the heavy metals and metalloids,
63
cadmium (Cd) ranks the first in the percentage of soil samples (7.0%) exceeding the MEP
64
limit.
65
Arable land per capita in China is less than half of the world average, so protecting
66
this precious resource from degradation and contamination has now been placed very high in
67
the government’s agenda 2. Large sums of public funding have also been promised for the
68
remediation of contaminated soils 3. However, how this should be done has been a subject of
69
intense debate. Here, we present an appraisal of China’s current status of soil contamination
70
and the effect on food safety, and propose strategies to deal with this worsening problem. The
71
focus of this policy analysis is on heavy metals and metalloids in agricultural soils, as these
72
can present a serious threat to human health through the food chain. Special emphasis is
4
ACS Paragon Plus Environment
Page 4 of 31
Page 5 of 31
Environmental Science & Technology
73
placed on Cd, as it is the most critical toxic metal threatening food safety and agricultural
74
sustainability in China.
75
Soil quality standards in China
76
Because heavy metals and metalloids in soils are derived from both natural and
77
anthropogenic sources, it is not straight forward to determine if a soil is contaminated. In the
78
recent MEP/MLR soil contamination survey, the status of soil contamination was determined
79
by comparing the total concentration of a contaminant to the benchmark values of the
80
Chinese environmental quality standard for soils issued by the MEP in 1995. The standard
81
specifies three classes of benchmark values for eight heavy metals or metalloids and two
82
pesticides 4 (Table 1). Class I values are considered to represent the natural background, to be
83
used in the protection of regional natural ecosystems from contamination. Class II is set up to
84
protect agricultural production and human health via the food chain, and can be applied to
85
agricultural, orchard and pasture land. The class II values are dependent on soil pH and land
86
use. In the recent MEP and MLR soil contamination survey, a soil is considered to be
87
contaminated if a heavy metal or metalloid is above the class II value; the degree of
88
contamination is designated as light, medium or severe when the concentration is 1 – 3, 3 – 5
89
or >5 times the benchmark value, respectively. Class III is for the protection of crops or
90
forests from phytotoxicity and may also be used where the natural background is elevated.
91
A number of issues have been raised with regard to the China’s soil quality standards.
92
First, for a country as large and geochemically diverse as China, natural background
93
concentrations of heavy metals and metalloids are not single values but are likely to vary
94
substantially across the country. Natural background levels depend on the soil parent
95
materials and pedogenetic processes, and therefore vary among different soil types 5-8. For
96
example, soils developed from serpentine rocks are naturally enriched with nickel and
97
chromium. The concentrations of several heavy metals are known to correlate closely with
98
those of iron or aluminum oxides in soils, reflecting the parallel influences of pedogensis on
99
these elements 5, 9. A pan-European comparison revealed higher background levels of several
100
heavy metals and metalloids in the more weathered soils of southern Europe than in the
101
younger soils of northern Europe, with the break in concentrations coinciding with the
102
maximum extent of the last glaciation 10. A national soil survey conducted in the early 1980s
103
showed that the 90th percentile Cd concentrations in both the A and C soil horizons were
104
markedly higher in Guizhou and Guangxi provinces in southwest China than in the other 5
ACS Paragon Plus Environment
Environmental Science & Technology
105
regions of China 11. Furthermore, soils developed from sedimentary parent materials,
106
particularly sedimentary limestone, tend to have higher Cd concentrations than others 11. In
107
the MEP/MLR soil contamination survey, soils with a high natural background of heavy
108
metals or metalloids would also be classified as “contaminated”.
109
Second, there are debates on whether the Class II values are over-protective or under-
110
protective. Recent studies using soil to plant transfer models suggest that the Class II Cd limit
111
may be set too low (i.e. over-protective) for soils with near neutral to alkaline pH 12, 13.
112
Certainly, the 0.3 – 0.6 mg kg-1 soil Cd limit (Table 1) is lower than either the 1 – 3 mg kg-1
113
limit adopted by the EU for land applications of sewage sludge or up to 39 mg kg-1 in the US-
114
EPA’s rules on land applications of biosolids 14. The EU risk assessment on Cd has derived
115
the predicted no effect concentrations (PNECs) of 0.6 – 2.3 mg kg-1 for the protection of
116
human health, mammals and bird, plants and soil organisms 15, whilst the US-EPA
117
recommends a screening value (ECOSSL) of 0.4 – 0.8 mg kg-1, above which further
118
investigations are needed to determine if a site might be hazardous 16 . In highly acidic soils,
119
however, food Cd limits may be exceeded even when soil Cd concentrations are below 0.3
120
mg kg-1 13. On the other hand, there is some evidence that the Class II Pb limits may be set
121
too high and may lead to non-compliance with the food Pb limits 17. The exposure pathway of
122
soil ingestion by humans is also not considered in setting the Pb limits.
123
Clearly, both issues would need to be addressed in any future revision of the soil
124
quality standards in China, taking into account evidence accumulated since the standard was
125
issued in 1995. When assessing the current status of soil contamination in China, it is
126
important to bear in mind the assessment is relative to the magnitude of the benchmark values
127
in the soil quality standard and some of the “contaminated” soils are due to naturally high
128
background concentrations.
129 130 131
The current status of soil contamination in China An important reason for the high percentages of Chinese soils identified as being
132
contaminated with Cd (7%) is because of the low Class II values: 0.3 and 0.6 mg kg-1 for
133
soils with pH 7.5, respectively (Table 1). Other countries may have higher Cd
134
concentrations in their soils, compared with the recent soil survey results in China. For
135
example, a national soil inventory shows that 45% and 20% of the soils in England and 6
ACS Paragon Plus Environment
Page 6 of 31
Page 7 of 31
Environmental Science & Technology
136
Wales exceed 0.3 and 0.6 mg kg-1, respectively 18. In continental Europe, the 75th percentile
137
value of soil Cd was found to be 0.27 and 0.32 mg kg-1 for soils from agricultural and grazing
138
land, respectively 10, which means that a considerable proportion of European soils is over
139
0.3 mg kg-1 limit. In the US, the 75th percentile for agricultural areas was 0.34 mg kg-1 19.
140
These comparisons help to place the current status of soil contamination in China in a
141
different perspective: in terms of the total concentrations it is not worse than other regions
142
such as Europe and the US. In the case of Ni, the relatively high percentage of contamination
143
in China (4.8%, Table 1) is also due to, at least partly, the Class II values being set close to
144
the Class I (natural background) level. On the other hand, the relatively low percentages of
145
soil samples identified as being contaminated with Pb or Cr (Table 1) can be attributed to the
146
large Class II values in the soil quality standard.
147
Whilst the current status of soil contamination in China may not be as grim as
148
perceived in popular media, there are reasons for concern. This is because large quantities of
149
heavy metals and metalloids have been discharged into the environment over the last three
150
decades coinciding with rapid industrialization and urbanization in China. In 2012, 22 billion
151
tons of waste water, 64 trillion cubic meters of waste gas and 3.3 billion tons of solid waste
152
were discharged from industrial sources in China 20. The total amount of five heavy metals
153
and metalloids (Hg, Cd, Cr, Pb and As) discharged in industrial waste water reached 441 tons
154
in 2012, although the discharge has been decreasing during recent years (Fig. 1). The
155
amounts of heavy metals released from mining are not quantified, but are probably
156
substantially higher. In 2010, China consumed 3.38 billion tons of coal 21, which is likely to
157
emit approximately 9000, 360, 450 and 25000 tons of As, Cd, Hg and Pb, respectively, based
158
on the average concentrations of these metals in coal and their emission factors 22. China is
159
also the largest producer and consumer of many heavy metals in the world. For example,
160
China produces and consumes about a third of the refinery cadmium in the world, most of it
161
being used in the production of nickel-cadmium batteries 23. Uncontrolled discharges of
162
waste water, gas and solids have cumulatively raised the burden of heavy metals in the
163
environment. A comparison between nationwide soil surveys conducted recently and those in
164
the late 1980s shows clear increases in the total concentrations of a number of heavy metals
165
and metalloids during the 25-year period. For example, average soil Cd concentrations
166
increased by 10 – 40% in the western and northern China and by over 50% in the coastal
167
region and the southwest of the country 24. Based on the inventory of inputs and outputs in
168
agricultural systems not subjected to serious contaminations from point-sources, Luo et al. 22 7
ACS Paragon Plus Environment
Environmental Science & Technology
169
estimated that the Cd concentration in Chinese agricultural soils has been increasing at an
170
average rate of 0.004 mg Cd kg-1 year-1. This is much greater than those reported elsewhere,
171
e.g. 0.00033 mg Cd kg-1 year-1 in Europe 25, and would lead to a doubling of the average soil
172
Cd concentration in China in 50 years if the input/output trend continued. Clearly, such an
173
increase rate is worrying and must be reduced as soon and as much as possible. For
174
comparison, it would take between 364 and 2433 years for the average concentrations of
175
other heavy metals or metalloids in soil to increase from their background levels to the Class
176
II limits 22. Therefore, Cd stands out as the most critical heavy metal for agricultural soils in
177
China.
178 179 180
Heavy metals and metalloids in food crops For heavy metals such as Cd to which the general population is exposed mainly
181
through the food chain 25, keeping the metal concentrations in the edible parts of agricultural
182
crops in check is an important and urgent task in China. An apparent paradox emerges when
183
the soil-crop data in China and the UK are compared. Whilst soil Cd concentrations in the
184
UK are generally higher than those in China, wheat grain produced in the UK rarely exceeds
185
the 0.2 mg Cd kg-1 limit of EU and FAO/WHO; exceedance was found in less than 0.2% of
186
survey samples analyzed 26, 27. In contrast, rice, the most important crop grown in southern
187
China, appears to be problematic in meeting the 0.2 mg Cd kg-1 limit of the Chinese food
188
standard. In some areas of southern China, particularly those impacted by mining and
189
industrial activities, considerable proportions of rice grain exceed the Cd limit 28, causing
190
widespread public concern in recent years. A recent survey of rice grain from a county
191
located in the Xiangjiang river basin in Hunan province, one of the most important rice
192
growing areas in China, showed that 60% of the samples exceed the 0.2 mg Cd kg-1 limit, and
193
11% contain >1.0 mg Cd kg-1 29. On a countrywide scale, market basket surveys reported
194
between 2 and 13% of rice grain samples exceeding the limit 30-32.
195
China has adopted a food standard limit of 0.2 mg Cd kg-1, which is stricter than the
196
FAO/WHO’s limit of 0.4 mg kg-1 for rice 33. This strict limit is deemed necessary because of
197
the high consumption of rice by Chinese population: 238 and 327 g day-1 for national average
198
and southern population average, respectively 34. Cd intake from rice alone with a Cd
199
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
ACS Paragon Plus Environment
Page 8 of 31
Page 9 of 31
Environmental Science & Technology
200
national average (for adults of 65 kg body weight); the latter already exceeds the FAO/WHO
201
tolerable daily intake (TDI) of 0.83 µg kg-1 body weight day-1 35. For populations based on a
202
subsistence rice diet, Cd in rice may pose a greater risk to humans because of the generally
203
low concentrations of Fe and Zn in the diet, which could result in greater uptake of Cd 36, and
204
such populations typically consume large amounts of rice (~500 g day-1). Moreover, residents
205
living in contaminated areas who consume mainly locally produced grain and vegetables are
206
particularly vulnerable. A number of studies have shown that the dietary Cd intake for
207
residents in some mining impacted areas in China is well over the TDI level, with rice being
208
the most important source 37-40. In some cases the daily Cd intake exceeds 300 µg day-1 (4.6
209
µg kg-1 body weight day-1), which is likely to cause severe chronic Cd poisoning 41. There is
210
also strong evidence linking elevated exposure to Cd with renal dysfunction and osteoporosis,
211
and increased cancer mortality rate in populations impacted by mining activities in China 38,
212
42-47
213
. Apart from Cd, accumulation of As and Pb in rice is also of concern. A survey of rice
214
grain collected from mining-impacted paddy fields in Hunan province showed that 65, 50,
215
and 34% of the samples fail the national food standards for Cd, As, and Pb, respectively 28, 48.
216
Rice grain produced in a Hg mining and smelting area in Guizhou, southwest China, also
217
contains significant amounts of methylmercury, a highly toxic species of Hg 49.
218
Approximately a third of the local farmers in the area had a methylmercury intake exceeding
219
the reference dose of 0.1 µg kg-1 bw day-1 established by the U.S. Environmental Protection
220
Agency, with rice contributing to 95% of the intake 50.
221 222 223
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
224
than in other regions for a number of reasons. First, mining of base metals and metal smelting
225
have been important economic activities in some parts of southern China for a long time.
226
These activities have released large quantities of heavy metals and metalloids into the
227
environment due to inadequate enforcement of environmental protection law. Taking Hunan
228
province (the largest rice producing province in China) as an example, it has been estimated
229
that mining, smelting and other industries released 610, 31, 136 and 4 tons year-1 of Pb, Cd,
230
Cr and Hg, respectively, into the Xiangjiang river, a major tributary of the Yangtze River 51. 9
ACS Paragon Plus Environment
Environmental Science & Technology
231
Xiangjiang river basin is an important rice producing area, but is also among the most
232
contaminated areas in China 52. Some stream water in the Xiangjiang River catchment area
233
contains as much as 40 µg Cd L-1, 8 times the drinking water limit 29, whilst Liu et al. 51
234
reported maximum concentrations of 430 µg Cd L-1, 500 µg As L-1 and 138 µg Pb L-1 in
235
some sections of Xiangjiang river. As the double-rice cropping system, a typical cropping
236
system in southern China, consumes large quantities irrigation water, inputs of heavy metals
237
into the soil can be substantial. Assuming 1 m irrigation water per year, the input of Cd into
238
the paddy system would amount to 50, 100 and 400 g ha-1, respectively, with Cd
239
concentrations in water of 5, 10 and 40 µg L-1 (these concentrations correspond to the
240
drinking water limit, irrigation water limit and the highest concentration reported by Du et
241
al.29, respectively). These inputs could raise the Cd concentration in the topsoil (0-20 cm) by
242
0.02, 0.04 and 0.15 mg kg-1, respectively, in a single year if there were no losses of Cd from
243
the system. Based on the typical biomass (12 tons ha-1 for grain and straw, respectively, for
244
early and late rice) and the range of Cd concentrations in rice grain (0.05 – 0.5 mg kg-1) and
245
straw (0.4 – 4 mg kg-1) in southern China, crop uptake is likely to remove 5 – 55 g ha-1of Cd
246
from the soil depending on the status of Cd contamination in the paddy field (Table 2), i.e.
247
only about one tenth of the Cd inputs from irrigation water. There are other sources of heavy
248
metals and metalloids, such as atmospheric deposition, fertilizers and manures (Table 2). Due
249
to metal smelting and coal combustion, the rates of atmospheric deposition in China are
250
higher than those in developed countries 22. Atmospheric deposition of Cd ranges from 0.4 to
251
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
252
current mean of EU of 0.35 g ha-1 yr-1 53. Phosphate fertilizers can contain considerable
253
amounts of Cd. But fortunately, many rock phosphates in China have low levels of Cd and
254
consequently, home-produced phosphate fertilizers are not an important source of Cd to
255
agricultural soils, although some imported phosphate fertilizers used to make compound
256
fertilizers may be elevated in Cd 22, 54. Some organic manures contain high levels of heavy
257
metals or metalloids, especially Zn, Cu, As and occasionally, Cd 22. Where sewage sludge is
258
applied onto agricultural land, it could also add significant amounts of heavy metals,
259
especially Zn and Cu 22. The data for losses of heavy metals through runoff and leaching are
260
scarce, making mass balance calculations difficult. However, it is apparent from Table 2 that
261
irrigation is the dominant source of Cd in the double rice cropping system in southern China
262
if the water used contains elevated levels of Cd.
10
ACS Paragon Plus Environment
Page 10 of 31
Page 11 of 31
Environmental Science & Technology
263
The second important reason causing high accumulation of cationic heavy metals in
264
rice and vegetables is the acidic nature of the soils in many areas of southern China, leading
265
to a high phytoavailability of Cd in the soil. In the tropical and subtropical regions of
266
southern China, red soil and the paddy soil developed from this soil type are inherently acidic.
267
Use of acidifying nitrogen fertilizers, crop uptake of base cations and acid deposition from
268
the atmosphere have contributed to significant soil acidification in major croplands in China
269
over the last three decades 55. Approximately half of the paddy soils in Hunan province have
270
a pH lower than 5.5. Several field or pot studies have shown that paddy soil pH has a highly
271
significant effect on the accumulation Cd in rice grain 13, 56, 57. Based on the regression model
272
presented by Romkens et al. 56, it can be predicted that for Indica rice cultivars which are
273
commonly grown in southern China, grain Cd may exceed the 0.2 mg kg-1 limit when soil Cd
274
concentration is above 0.18 and 0.9 mg kg-1 at soil pHs of 5 and 7, respectively (Fig. 2). This
275
model prediction corroborates anecdotal evidence that exceedance of the grain Cd limit
276
occurs on some “uncontaminated” soils, most likely due to acidic pH. Upon flooding in
277
paddy systems, the soil pH increases to the neutral range, thus limiting Cd phytoavailability
278
in the soil. However, water is normally drained during the late tillering stage to control
279
infertile tillers and also during the grain filling stages to facilitate harvesting. Rain-fed paddy
280
fields may also be subjected to drought periods. Soil pH drops and Cd phytoavailability
281
increases when the water is drained away, resulting in a massive increase in Cd uptake by
282
rice plants 58. Formation of cadmium sulfide under anaerobic conditions renders Cd less
283
phytoavailable, but oxidation of cadmium sulfide upon water draining is also rapid 59, 60. In
284
addition, Mn2+ accumulated in soil solution under flooded conditions, which can inhibit Cd
285
uptake by rice roots via the OsNRAMP5 transporter 61. Under aerobic conditions, soluble
286
Mn2+ is oxidized, thus removing an important inhibitor of Cd uptake. It is well known that
287
growing rice under flooded conditions can reduce excessive Cd accumulation 62, 63. However,
288
this is not always possible, due to the reasons described above. Moreover, continuous
289
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
290 291
of the Indica cultivars grown in southern China happen to be Cd accumulators. In general
292
Indica cultivars tend to accumulate more Cd in the grain than Japonica cultivars that are
293
adapted to the temperate region, although within each type there is substantial variation 56, 66,
294
67
295
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
ACS Paragon Plus Environment
Environmental Science & Technology
296
latter exceedance is predicted with a soil total Cd of 0.55 and 1.7 mg kg-1 at pH 5 and 7,
297
respectively (Fig. 2). On acidic soils, some vegetables, such as carrot, leafy, brassica and
298
solanaceous vegetables, are also prone to Cd accumulation 13, 68-70, therefore adding to the
299
dietary Cd intake of the local residents 70-72.
300
So, the combination of soil contamination, high phytoavailability in acidic soils and
301
cultivation of heavy metal accumulating rice cultivars and vegetable species substantially
302
increases the risk of the transfer of heavy metals from soil to the food chain in southern China.
303
Under these conditions, naturally elevated concentrations of heavy metals may pose a risk
304
similar to those from anthropogenic activities. The last two factors discussed above probably
305
also explain why such risk is higher in southern China than in Europe at the same level of
306
total metal concentration in soil.
307 308 309
Strategies to mitigate heavy metal contamination in food crops Urgent measures are needed to mitigate the serious problem of heavy metal or
310
metalloid contamination in food crops in China, some of which are discussed below.
311
Implementation of various strategies requires not only technological advances, but also
312
social-economic evaluation and effective enforcement of environmental protection law, as
313
well as government subsidy.
314
Identify and stop the sources of contamination. The first step to combat heavy metal
315
contamination in the soil-plant systems is to identify and stop the main sources of
316
contamination. This requires more stringent monitoring and effective enforcement of
317
environmental protection law, especially with regard to large emission sources such as
318
mining, smelting and other metal consuming industries. There is an urgent need to establish
319
national and regional inventories of metal and metalloid concentrations in water used for
320
irrigation and of atmospheric inputs. This would enable realistic appraisal of the current
321
contamination status and prediction of the future trend. Where irrigation water contains
322
elevated levels of metals or metalloids, simple and effective techniques should be developed
323
to remove the contaminants before water reaches the field; where this is not possible,
324
alternative clean water sources would need to be found. Starting in 2011, the Chinese
325
government has initiated two large national programs to combat heavy metal pollution: the
326
12th five-year plan for preventing heavy metal pollution and the Xiangjiang river basin 12
ACS Paragon Plus Environment
Page 12 of 31
Page 13 of 31
Environmental Science & Technology
327
control plan for heavy metal pollution, each with funding of tens of billions of Chinese Yuan
328
52
329
discharge of five heavy metals and metalloids (Hg, Cd, As, Cr, Pb) in key regions (East and
330
Central China) by 15% by 2015 from the 2007 base and to control the discharge in non-key
331
regions below the 2007 level. The second program aims to reduce the number of heavy-metal
332
polluting enterprises and the amount of heavy metal emissions in the Xiangjiang river basin
333
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
ACS Paragon Plus Environment
Environmental Science & Technology
359
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
ACS Paragon Plus Environment
Page 14 of 31
Page 15 of 31
Environmental Science & Technology
391
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
.
15
ACS Paragon Plus Environment
Environmental Science & Technology
420
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
ACS Paragon Plus Environment
Page 16 of 31
Page 17 of 31
Environmental Science & Technology
450
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
REFERENCES:
454
(1)
455
Report on the national soil contamination survey.
456
http://www.mep.gov.cn/gkml/hbb/qt/201404/t20140417_270670.htm. (27th August 2014),
457
(2)
458
http://www.mlr.gov.cn/xwdt/jrxw/201211/t20121101_1152706.htm. (27th August 2014),
459
(3)
460
http://www.npc.gov.cn/npc/zhibo/zzzb22/2011-10/25/content_1676505.htm. (10/9/2014),
461
(4)
462
GB 15618-1995. In 1995.
463
(5)
464
concentrations of trace metals in soils for risk assessment. Environ. Pollut. 2007, 148 (1),
465
221-229.
466
(6)
467
Environ. 2005, 350 (1-3), 12-27.
468
(7)
469
for elements in the environment: regional geochemical surveys versus enrichment factors. Sci.
470
Total Environ. 2005, 337 (1-3), 91-107.
471
(8)
472
R. M. Methodology for the determination of normal background concentrations of
473
contaminants in English soil. Sci. Total Environ. 2013, 454-455, 604-618.
474
(9)
475
A.; Cozens, G.; Radford, N.; Bettenay, L. Geochemical indices allow estimation of heavy
476
metal background concentrations in soils. Glob. Biogeochem. Cycle 2004, 18 (1), GB1014.
477
(10)
478
Europe and Australia: Demonstrating comparability, identifying continental-scale processes
479
and learning lessons for global geochemical mapping. Sci. Total Environ. 2012, 416, 239-252.
480
(11)
481
Chinese soils (in Chinese). Chinese Environmental Science Publisher: Beijing, 1990.
The Ministry of Environmental Protection; The Ministry of Land and Resources
The Ministry of Land and Resources
The National People's Congress of the People's Republic of China
National Environmental Protection Bureau Environmental quality standard for soils
Zhao, F. J.; McGrath, S. P.; Merrington, G. Estimates of ambient background
Reimann, C.; Garrett, R. G. Geochemical background - concept and reality. Sci. Total
Reimann, C.; de Caritat, P. Distinguishing between natural and anthropogenic sources
Ander, E. L.; Johnson, C. C.; Cave, M. R.; Palumbo-Roe, B.; Nathanail, C. P.; Lark,
Hamon, R. E.; McLaughlin, M. J.; Gilkes, R. J.; Rate, A. W.; Zarcinas, B.; Robertson,
Reimann, C.; de Caritat, P.; Team, G. P.; Team, N. P. New soil composition data for
Chinese Environmental Monitoring Station Background concentrations of elements in
17
ACS Paragon Plus Environment
Environmental Science & Technology
482
(12)
Ding, C.; Zhang, T.; Wang, X.; Zhou, F.; Yang, Y.; Huang, G. Prediction model for
483
cadmium transfer from soil to carrot (Daucus carota L.) and its application to derive soil
484
thresholds for food safety. J. Agric. Food Chem. 2013, 61 (43), 10273-10282.
485
(13)
486
As, Cd and Pb uptake by rice and vegetables using field data from China. J. Environ. Sci. -
487
China 2011, 23 (1), 70-78.
488
(14)
489
sludge: Scientific perspectives of heavy metal loading limits in Europe in the United States.
490
Environ. Rev. 1994, 2 (1), 108-118.
491
(15)
492
environment (Vol. 72). ; Office for Official Publications of the European Communities:
493
Luxembourg, 2007.
494
(16)
495
Directive 9285.7-65); United States Environmental Protection Agency: Washington, 2005.
496
(17)
497
genotype on lead concentration in rootstalk vegetables and the selection of cultivars for food
498
safety. J. Environ. Manag. 2013, 122, 8-14.
499
(18)
500
Ingham, M.; Gowing, C.; Carter, S. The advanced soil geochemical atlas of England and
501
Wales. www.bgs.ac.uk/gbase/advsoilatlasEW.html. British Geological Survey: Keyworth,
502
2012.
503
(19)
504
zinc, copper, and nickel in agricultural soils of the United States of America. J. Environ. Qual.
505
1993, 22 (2), 335-348.
506
(20)
507
2013. China Environment Yearbook Publisher: Beijing, 2013; Vol. 24.
508
(21)
509
2011. China Environment Yearbook Publisher: Beijing, 2011; Vol. 22.
510
(22)
511
element inputs to agricultural soils in China. J. Environ. Manag. 2009, 90 (8), 2524-2530.
512
(23)
U. S. Geological Survey 2012 Minerals Yearbook, Cadmium; 2013.
513
(24)
The Ministry of Land and Resources
514
http://www.mlr.gov.cn/xwdt/jrxw/201404/t20140417_1312999.htm. (10/9/2014),
Zhang, H. Z.; Luo, Y. M.; Song, J.; Zhang, H. B.; Xia, J. Q.; Zhao, Q. G. Predicting
McGrath, S. P.; Chang, A. C.; Page, A. L.; Witter, E. Land application of sewage
European Union European Union risk assessment report. Cadmium metal. Part I
US-EPA Ecological soil screening levels for Cadmium (Interim Final, OSWER
Ding, C.; Zhang, T.; Wang, X.; Zhou, F.; Yang, Y.; Yin, Y. Effects of soil type and
Rawlins, B. G.; McGrath, S. P.; Scheib, A. J.; Breward, N.; Cave, M.; Lister, T. R.;
Holmgren, G. G. S.; Meyer, M. W.; Chaney, R. L.; Daniels, R. B. Cadmium, lead,
China Environment Yearbook Editorial Committee China Environment Yearbook
China Environment Yearbook Editorial Committee China Environment Yearbook
Luo, L.; Ma, Y. B.; Zhang, S. Z.; Wei, D. P.; Zhu, Y. G. An inventory of trace
18
ACS Paragon Plus Environment
Page 18 of 31
Page 19 of 31
Environmental Science & Technology
515
(25)
Smolders, E.; Mertens, J. Chapter 10. Cadmium. In Heavy Metals in Soils: Trace
516
Metals and Metalloids in Soils and their Bioavailability, Alloway, B. J., Ed. Springer
517
Science+Business Media Dordrecht, 2013; pp 283-311.
518
(26)
519
British wheat grain. J. Environ. Qual. 1995, 24 (5), 850-855.
520
(27)
521
the potential to lead to exceedance of maximum limit concentrations of contaminants in food
522
and feed. Soil Use Manage. 2014, doi: 10.1111/sum.12080.
523
(28)
524
Zhu, Y. G. Occurrence and partitioning of cadmium, arsenic and lead in mine impacted
525
paddy rice: Hunan, China. Environ. Sci. Technol. 2009, 43 (3), 637-642.
526
(29)
527
activities on Cd pollution to the paddy soils and rice grain in Hunan province, Central South
528
China. Environ. Monit. Assess. 2013, 185 (12), 9843-9856.
529
(30)
530
cadmium, lead, mercury and arsenic in Chinese market milled rice and associated population
531
health risk. Food Control 2010, 21 (12), 1757-1763.
532
(31)
533
Zhu, X.; Hu, Q. Concentrations and health risks of lead, cadmium, arsenic, and mercury in
534
rice and edible mushrooms in China. Food Chem. 2014, 147, 147-151.
535
(32)
536
rice samples from some Chinese open markets and their relevance to food safety. Journal of
537
Safety and Environment 2008, 8, 119-122 (in Chinese).
538
(33)
539
Alimentarius Commission (ALINORM 06/29/41); Codex Alimentarius Commission: Rome,
540
2006.
541
(34)
542
Chinese food and its cancer risk. Environ. Inter. 2011, 37 (7), 1219-1225.
543
(35)
544
Committee on Food Additives seventy-third meeting,
545
http://www.who.int/foodsafety/publications/chem/summary73.pdf; World Health Organization:
546
Geneva, 2010.
Chaudri, A. M.; Zhao, F. J.; McGrath, S. P.; Crosland, A. R. The Cadmium content of
McGrath, S. P.; Zhao, F. J. Concentrations of metals and metalloids in soils that have
Williams, P. N.; Lei, M.; Sun, G. X.; Huang, Q.; Lu, Y.; Deacon, C.; Meharg, A. A.;
Du, Y.; Hu, X. F.; Wu, X. H.; Shu, Y.; Jiang, Y.; Yan, X. J. Affects of mining
Qian, Y. Z.; Chen, C.; Zhang, Q.; Li, Y.; Chen, Z. J.; Li, M. Concentrations of
Fang, Y.; Sun, X.; Yang, W.; Ma, N.; Xin, Z.; Fu, J.; Liu, X.; Liu, M.; Mariga, A. M.;
Zhen, Y. H.; Cheng, Y. J.; Pan, G. X.; Li, L. Q. Cd, Zn and Se content of the polished
Codex Alimentarius Commission Report of the 29th session of the Codex
Li, G.; Sun, G. X.; Williams, P. N.; Nunes, L.; Zhu, Y. G. Inorganic arsenic in
Joint FAO/WHO Expert Committee on Food Additives Joint FAO/WHO Expert
19
ACS Paragon Plus Environment
Environmental Science & Technology
547
(36)
Chaney, R. L. Food safety issues for mineral and organic fertilizers. Adv. Agron. 2012,
548
117, 51-116.
549
(37)
550
Regional assessment of cadmium pollution in agricultural lands and the potential health risk
551
related to intensive mining activities: A case study in Chenzhou City, China. J. Environ. Sci. -
552
China 2008, 20 (6), 696-703.
553
(38)
554
effects: A 19-year follow-up study of a polluted area in China. Sci. Total Environ. 2014, 470,
555
224-228.
556
(39)
557
area contaminated by irrigation water in China. B World Health Organ 1995, 73 (3), 359-367.
558
(40)
559
assessment of heavy metals in the population near mining area in South China. PloS One
560
2014, 9 (4), e94484-e94484.
561
(41)
562
Skerfving, S. Non-renal effects and the risk assessment of environmental cadmium exposure.
563
Environ. Health Persp. 2014, 122, 431-438.
564
(42)
565
Bernard, A. Osteoporosis and renal dysfunction in a general population exposed to cadmium
566
in China. Environ. Res. 2004, 96 (3), 353-359.
567
(43)
568
Wang, Z. J.; Li, P. J.; Lundstrom, N. G.; Li, Y. D.; Nordberg, G. F. Cadmium biomonitoring
569
and renal dysfunction among a population environmentally exposed to cadmium from
570
smelting in China (ChinaCad). Biometals 2002, 15 (4), 397-410.
571
(44)
572
contamination of irrigation water: dose-response analysis in a Chinese population. B World
573
Health Organ 1998, 76 (2), 153-159.
574
(45)
575
J.; Zhong, A. M.; Ling, W. H. Cancer mortality in a Chinese population surrounding a multi-
576
metal sulphide mine in Guangdong province: an ecologic study. BMC Public Health 2011, 11
577
(319), 1-15.
Zhai, L. M.; Liao, X. Y.; Chen, T. B.; Yan, X. L.; Xie, H.; Wu, B.; Wang, L. X.
Zhang, W. L.; Du, Y.; Zhai, M. M.; Shang, Q. Cadmium exposure and its health
Cai, S.; Yue, L.; Shang, Q.; Nordberg, G. Cadmium exposure among residents in an
Zhuang, P.; Lu, H.; Li, Z.; Zou, B.; McBride, M. B. Multiple exposure and effects
Åkesson, A.; Barregard, L.; Bergdahl, I. A.; Nordberg, G. F.; Nordberg, M.;
Jin, T. Y.; Nordberg, G.; Ye, T. T.; Bo, M. H.; Wang, H. F.; Zhu, G. Y.; Kong, Q. H.;
Jin, T. Y.; Nordberg, M.; Frech, W.; Dumont, X.; Bernard, A.; Ye, T. T.; Kong, Q. H.;
Cai, S.; Yue, L.; Jin, T.; Nordberg, G. Renal dysfunction from cadmium
Wang, M.; Song, H.; Chen, W. Q.; Lu, C. Y.; Hu, Q. S.; Ren, Z. F.; Yang, Y.; Xu, Y.
20
ACS Paragon Plus Environment
Page 20 of 31
Page 21 of 31
Environmental Science & Technology
578
(46)
Nordberg, G.; Jin, T. Y.; Bernard, A.; Fierens, S.; Buchet, J. P.; Ye, T. T.; Kong, Q.
579
H.; Wang, H. F. Low bone density and renal dysfunction following environmental cadmium
580
exposure in China. Ambio 2002, 31 (6), 478-481.
581
(47)
582
metal mixtures and human health impacts in a contaminated area in Nanning, China. Environ.
583
Inter. 2005, 31 (6), 784-790.
584
(48)
585
Carey, A. M.; Deacon, C.; Raab, A.; Meharg, A. A.; Williams, P. N. High percentage
586
inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ. Sci.
587
Technol. 2008, 42 (13), 5008-5013.
588
(49)
589
M.; Bai, W. Y.; Li, Z. G.; Fu, X. W. Human exposure to methylmercury through rice intake
590
in mercury mining areas, Guizhou province, China. Environ. Sci. Technol. 2008, 42 (1), 326-
591
332.
592
(50)
593
rather than fish, is the major pathway for methylmercury exposure. Environ. Health Persp.
594
2010, 118 (9), 1183-1188.
595
(51)
596
metals pollution status and reasons in Xiangjiang river and discussion on its countermeasures
597
(in Chinese). Environ. Protect. Sci. 2010, 36 (4), 26-29.
598
(52)
599
pollution-control policies and countermeasures. Sustainability 2014, 6, 5820-5838.
600
(53)
601
cadmium fluxes to European agricultural soils. Sci. Total Environ. 2014, 485-486, 319-328.
602
(54)
603
phosphate fertilizers of China and their effects on ecological environment. Acta Pedolog. Sin.
604
1992, 29, 150-157.
605
(55)
606
Goulding, K. W. T.; Vitousek, P. M.; Zhang, F. S. Significant acidification in major Chinese
607
croplands. Science 2010, 327 (5968), 1008-1010.
608
(56)
609
G. F. Prediction of cadmium uptake by brown rice and derivation of soil-plant transfer
610
models to improve soil protection guidelines. Environ. Pollut. 2009, 157 (8-9), 2435-2444.
Cui, Y. J.; Zhu, Y. G.; Zhai, R. H.; Huang, Y. Z.; Qiu, Y.; Liang, J. Z. Exposure to
Zhu, Y. G.; Sun, G. X.; Lei, M.; Teng, M.; Liu, Y. X.; Chen, N. C.; Wang, L. H.;
Feng, X. B.; Li, P.; Qiu, G. L.; Wang, S.; Li, G. H.; Shang, L. H.; Meng, B.; Jiang, H.
Zhang, H.; Feng, X. B.; Larssen, T.; Qiu, G. L.; Vogt, R. D. In inland China, rice,
Liu, Y. C.; Gao, S.; Li, Z. G.; Liu, S. Q.; Huang, K. L.; Li, J. S. Analysis on heavy
Hu, H.; Jin, Q.; Kavan, P. A study of heavy metal pollution in China: current status,
Six, L.; Smolders, S. Future trends in soil cadmium concentration under current
Lu, R. K.; Shi, Z. Y.; Xiong, L. M. Cadmium contents of rock phosphates and
Guo, J. H.; Liu, X. J.; Zhang, Y.; Shen, J. L.; Han, W. X.; Zhang, W. F.; Christie, P.;
Römkens, P. F. A. M.; Guo, H. Y.; Chu, C. L.; Liu, T. S.; Chiang, C. F.; Koopmans,
21
ACS Paragon Plus Environment
Environmental Science & Technology
611
(57)
Ye, X. X.; Li, H. Y.; Ma, Y. B.; Wu, L.; Sun, B. The bioaccumulation of Cd in rice
612
grains in paddy soils as affected and predicted by soil properties. J. Soils Sed. 2014, 14 (8),
613
1407-1416.
614
(58)
615
capable of accumulating Cd at high levels: Reduction of Cd content of rice grain. Environ.
616
Sci. Technol. 2009, 43 (15), 5878-5883.
617
(59)
618
Speciation and release kinetics of cadmium in an alkaline paddy soil under various flooding
619
periods and draining conditions. Environ. Sci. Technol. 2011, 45 (10), 4249-4255.
620
(60)
621
solubility and solid-phase speciation in a paddy soil as affected by reducible sulfate and
622
copper. Environ. Sci. Technol. 2013, 47 (22), 12775-12783.
623
(61)
624
Zhao, F. J.; Huang, C. F.; Lian, X. M. OsNRAMP5 contributes to manganese translocation
625
and distribution in rice shoots J. Exp. Bot. 2014, 65, 4849-4861.
626
(62)
627
Luo, Y. M.; Christie, P.; Wu, L. H. Effect of water management on cadmium and arsenic
628
accumulation by rice (Oryza sativa L.) with different metal accumulation capacities. J. Soil
629
Sed. 2013, 13 (5), 916-924.
630
(63)
631
management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations
632
in Japanese rice. Environ. Sci. Technol. 2009, 43 (24), 9361-9367.
633
(64)
634
accumulation in rice with water management and silicon fertilization. Environ. Sci. Technol.
635
2009, 43, 3778-3783.
636
(65)
637
decreases arsenic accumulation. Environ. Sci. Technol. 2008, 42, 5574–5579.
638
(66)
639
trait locus controlling cadmium translocation in rice (Oryza sativa). New Phytol. 2009, 182
640
(3), 644-653.
641
(67)
642
cadmium accumulation among rice cultivars and types and the selection of cultivars for
643
reducing cadmium in the diet. J. Sci. Food Agric. 2005, 85 (1), 147-153.
Murakami, M.; Nakagawa, F.; Ae, N.; Ito, M.; Arao, T. Phytoextraction by rice
Khaokaew, S.; Chaney, R. L.; Landrot, G.; Ginder-Vogel, M.; Sparks, D. L.
Fulda, B.; Voegelin, A.; Kretzschmar, R. Redox-controlled changes in cadmium
Yang, M.; Zhang, Y. Y.; Zhang, L.; Hu, J.; Zhang, X.; Lu, K.; Dong, H.; Wang, D.;
Hu, P. J.; Li, Z.; Yuan, C.; Ouyang, Y. N.; Zhou, L. Q.; Huang, J. X.; Huang, Y. J.;
Arao, T.; Kawasaki, A.; Baba, K.; Mori, S.; Matsumoto, S. Effects of water
Li, R. Y.; Stroud, J. L.; Ma, J. F.; McGrath, S. P.; Zhao, F. J. Mitigation of arsenic
Xu, X. Y.; McGrath, S. P.; Meharg, A.; Zhao, F. J. Growing rice aerobically markedly
Ueno, D.; Kono, I.; Yokosho, K.; Ando, T.; Yano, M.; Ma, J. F. A major quantitative
Liu, J. G.; Zhu, Q. S.; Zhang, Z. J.; Xu, J. K.; Yang, J. C.; Wong, M. H. Variations in
22
ACS Paragon Plus Environment
Page 22 of 31
Page 23 of 31
Environmental Science & Technology
644
(68)
Yang, J. X.; Guo, H. T.; Ma, Y. B.; Wang, L. Q.; Wei, D. P.; Hua, L. O. Genotypic
645
variations in the accumulation of Cd exhibited by different vegetables. J. Environ. Sci. -
646
China 2010, 22 (8), 1246-1252.
647
(69)
648
factors and predictions for cadmium transfer from the soil into spinach plants. Ecotox.
649
Environ. Safe. 2013, 93, 180-185.
650
(70)
651
the Chenzhou lead/zinc mine spill (Hunan, China). Sci. Total Environ. 2005, 339 (1-3), 153-
652
166.
653
(71)
654
Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China.
655
Environ. Inter. 2004, 30 (6), 785-791.
656
(72)
657
Cadmium in agricultural soils, vegetables and rice and potential health risk in vicinity of
658
Dabaoshan Mine in Shaoguan, China. Journal of Central South University 2014, 21 (5),
659
2004-2010.
660
(73)
661
S.; Chia, C.; Marjo, C.; Gong, B.; Munroe, P.; Donne, S. A three-year experiment confirms
662
continuous immobilization of cadmium and lead in contaminated paddy field with biochar
663
amendment. J. Hazard. Mat. 2014, 272, 121-128.
664
(74)
665
W.; Zhang, X. H.; Zheng, J. F.; Chang, A. Biochar soil amendment as a solution to prevent
666
Cd-tainted rice from China: Results from a cross-site field experiment. Ecol. Eng. 2013, 58,
667
378-383.
668
(75)
669
Zhang, X.-N. Sepiolite is recommended for the remediation of Cd-contaminated paddy soil.
670
Acta Agric. Scand. Sect. B-Soil Plant Sci. 2010, 60 (2), 110-116.
671
(76)
672
risk via rice consumption: A case study in Miaoqian village, Longyan, China. Environ. Inter.
673
2014, 68, 154-161.
674
(77)
675
phytoavailability decreased effectively by rape straw and/or red mud with zinc sulphate in a
676
Cd-contaminated calcareous soil. PloS One 2014, 9 (10), e109967.
Liang, Z. F.; Ding, Q.; Wei, D. P.; Li, J. M.; Chen, S. B.; Ma, Y. B. Major controlling
Liu, H. Y.; Probst, A.; Liao, B. H. Metal contamination of soils and crops affected by
Cui, Y. J.; Zhu, Y. G.; Zhai, R. H.; Chen, D. Y.; Huang, Y. Z.; Qiu, Y.; Liang, J. Z.
Wang, Z. X.; Hu, X. B.; Xu, Z. C.; Cai, L. M.; Wang, J. N.; Zeng, D.; Hong, H. J.
Bian, R.; Joseph, S.; Cui, L.; Pan, G.; Li, L.; Liu, X.; Zhang, A.; Rutlidge, H.; Wong,
Bian, R. J.; Chen, D.; Liu, X. Y.; Cui, L. Q.; Li, L. Q.; Pan, G. X.; Xie, D.; Zheng, J.
Zhu, Q.-H.; Huang, D.-Y.; Zhu, G.-X.; Ge, T.-D.; Liu, G.-S.; Zhu, H.-H.; Liu, S.-L.;
Khan, S.; Reid, B. J.; Li, G.; Zhu, Y. G. Application of biochar to soil reduces cancer
Li, B.; Yang, J.; Wei, D.; Chen, S.; Li, J.; Ma, Y. Field evidence of cadmium
23
ACS Paragon Plus Environment
Environmental Science & Technology
677
(78)
Pinson, S. R. M.; Tarpley, L.; Yan, W. G.; Yeater, K.; Lahner, B.; Yakubova, E.;
678
Huang, X. Y.; Zhang, M.; Guerinot, M. L.; Salt, D. E. World-wide genetic diversity for
679
mineral element concentrations in rice grain. Crop Sci. 2015, 55, 1-18.
680
(79)
681
cultivars to minimize cadmium accumulation. Sci. Total Environ. 2008, 390 (2-3), 301-310.
682
(80)
683
controlling cadmium concentration in brown rice (Oryza sativa). New Phytol. 2005, 168 (2),
684
345-350.
685
(81)
686
novel major quantitative trait locus controlling distribution of Cd between roots and shoots in
687
rice. Plant Cell Physiol. 2009, 50 (12), 2223–2233.
688
(82)
689
T.; Yano, M.; Ishikawa, S. Detection of QTLs to reduce cadmium content in rice grains using
690
LAC23/Koshihikari chromosome segment substitution lines. Breed. Sci. 2013, 63 (3), 284-
691
291.
692
(83)
693
Q.; Xue, D. W. Identification of quantitative trait loci for Cd and Zn concentrations of brown
694
rice grown in Cd-polluted soils. Euphytica 2011, 180 (2), 173-179.
695
(84)
696
of quantitative trait loci for cadmium accumulation and distribution in rice (Oryza sativa).
697
Genome 2013, 56 (4), 227-232.
698
(85)
699
Masaki, S.; Satoh, H.; Yamaguchi, M.; Sakurai, K.; Takahashi, H.; Satoh-Nagasawa, N.;
700
Watanabe, A.; Fujimura, T.; Akagi, H. A single recessive gene controls cadmium
701
translocation in the cadmium hyperaccumulating rice cultivar Cho-Ko-Koku. Theor. Appl.
702
Genet. 2010, 120 (6), 1175-1182.
703
(86)
704
Baxter, I.; Guerinot, M. L.; Salt, D. E. Mapping and validation of quantitative trait loci
705
associated with concentrations of 16 elements in unmilled rice grain. Theor. Appl. Genet.
706
2014, 127 (1), 137-165.
707
(87)
708
Pozniak, C. J. Targeted mapping of Cdu1, a major locus regulating grain cadmium
Grant, C. A.; Clarke, J. M.; Duguid, S.; Chaney, R. L. Selection and breeding of plant
Ishikawa, S.; Ae, N.; Yano, M. Chromosomal regions with quantitative trait loci
Ueno, D.; Koyama, E.; Kono, I.; Ando, T.; Yano, M.; Ma, F. J. Identification of a
Abe, T.; Nonoue, Y.; Ono, N.; Omoteno, M.; Kuramata, M.; Fukuoka, S.; Yamamoto,
Zhang, X. Q.; Zhang, G. P.; Guo, L. B.; Wang, H. Z.; Zeng, D. L.; Dong, G. J.; Qian,
Yan, Y.-F.; Lestari, P.; Lee, K.-J.; Kim, M. Y.; Lee, S.-H.; Lee, B.-W. Identification
Tezuka, K.; Miyadate, H.; Katou, K.; Kodama, I.; Matsumoto, S.; Kawamoto, T.;
Zhang, M.; Pinson, S. R. M.; Tarpley, L.; Huang, X.-Y.; Lahner, B.; Yakubova, E.;
Wiebe, K.; Harris, N. S.; Faris, J. D.; Clarke, J. M.; Knox, R. E.; Taylor, G. J.;
24
ACS Paragon Plus Environment
Page 24 of 31
Page 25 of 31
Environmental Science & Technology
709
concentration in durum wheat (Triticum turgidum L. var durum). Theor. Appl. Genet. 2010,
710
121 (6), 1047-1058.
711
(88)
712
Nakamura, T.; Kanamaru, K. A major QTL controlling seed cadmium accumulation in
713
soybean. Crop Sci. 2010, 50 (5), 1728-1734.
714
(89)
715
linkage map construction and QTL mapping of cadmium accumulation in radish (Raphanus
716
sativus L.). Theor. Appl. Genet. 2012, 125 (4), 659-670.
717
(90)
718
durum wheat genetic stocks near-isogenic for cadmium concentration. Crop Sci. 1997, 37 (1),
719
297-297.
720
(91)
721
responsible for manganese and cadmium uptake in rice. Plant Cell 2012, 24 (5), 2155-2167.
722
(92)
723
limiting cadmium accumulation in rice. Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (38), 16500-
724
16505.
725
(93)
726
A.; Kyozuka, J.; Ishikawa, S.; Fujiwara, T. Low-affinity cation transporter (OsLCT1)
727
regulates cadmium transport into rice grains. Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (52),
728
20959-20964.
729
(94)
730
Arao, T.; Nishizawa, N. K.; Nakanishi, H. Ion-beam irradiation, gene identification, and
731
marker-assisted breeding in the development of low-cadmium rice. Proc. Natl. Acad. Sci. U.
732
S. A. 2012, 109 (47), 19166-19171.
733
(95)
734
Huang, Y.; Luo, Y.; Christie, P. Water management affects arsenic and cadmium
735
accumulation in different rice cultivars. Environ. Geochem. Health 2013, 35 (6), 767-778.
736
(96)
737
Tang, Y.-T.; Morel, J.-L.; Qiu, R.-L. Mitigation effects of silicon rich amendments on heavy
738
metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil.
739
Chemosphere 2011, 83 (9), 1234-1240.
Benitez, E. R.; Hajika, M.; Yamada, T.; Takahashi, K.; Oki, N.; Yamada, N.;
Xu, L.; Wang, L.; Gong, Y.; Dai, W.; Wang, Y.; Zhu, X.; Wen, T.; Liu, L. Genetic
Clarke, J. M.; Leisle, D.; DePauw, R. M.; Thiessen, L. L. Registration of five pairs of
Sasaki, A.; Yamaji, N.; Yokosho, K.; Ma, J. F. Nramp5 is a major transporter
Ueno, D.; Yamaji, N.; Kono, I.; Huang, C. F.; Ando, T.; Yano, M.; Ma, J. F. Gene
Uraguchi, S.; Kamiya, T.; Sakamoto, T.; Kasai, K.; Sato, Y.; Nagamura, Y.; Yoshida,
Ishikawa, S.; Ishimaru, Y.; Igura, M.; Kuramata, M.; Abe, T.; Senoura, T.; Hase, Y.;
Hu, P.; Huang, J.; Ouyang, Y.; Wu, L.; Song, J.; Wang, S.; Li, Z.; Han, C.; Zhou, L.;
Gu, H.-H.; Qiu, H.; Tian, T.; Zhan, S.-S.; Deng, T.-H.-B.; Chaney, R. L.; Wang, S.-Z.;
25
ACS Paragon Plus Environment
Environmental Science & Technology
740
(97)
Liu, C.; Li, F.; Luo, C.; Liu, X.; Wang, S.; Liu, T.; Li, X. Foliar application of two
741
silica sols reduced cadmium accumulation in rice grains. J. Hazard. Mat. 2009, 161 (2-3),
742
1466-1472.
743
(98)
744
The effects of zinc fertilization on cadmium concentration in wheat grain. J. Environ. Qual.
745
1994, 23 (4), 705-711.
746
(99)
747
four metal-contaminated soils using the cadmium/zinc hyperaccumulator Sedum
748
plumbizincicola. Environ. Pollut. 2014, 189, 176-183.
749
(100) Yang, X. E.; Long, X. X.; Ye, H. B.; He, Z. L.; Calvert, D. V.; Stoffella, P. J.
750
Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species
751
(Sedum alfredii Hance). Plant Soil 2004, 259 (1-2), 181-189.
Oliver, D. P.; Hannam, R.; Tiller, K. G.; Wilhelm, N. S.; Merry, R. H.; Cozens, G. D.
Li, Z.; Wu, L.; Hu, P.; Luo, Y.; Zhang, H.; Christie, P. Repeated phytoextraction of
752
26
ACS Paragon Plus Environment
Page 26 of 31
Page 27 of 31
Environmental Science & Technology
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
27
ACS Paragon Plus Environment
Environmental Science & Technology
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
28
ACS Paragon Plus Environment
Page 29 of 31
Environmental Science & Technology
761
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.
29
ACS Paragon Plus Environment
Environmental Science & Technology
Page 30 of 31
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.
30
ACS Paragon Plus Environment
Page 31 of 31
Environmental Science & Technology
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.
31
ACS Paragon Plus Environment
