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Designing Cropping Systems for Metal-Contaminated Sites: A Review

August 2012
Pedosphere 22(4):470-488

August 2012
22(4):470-488

DOI:10.1016/S1002-0160(12)60032-0

Authors:

Ye-Tao Tang

Sun Yat-Sen University

Teng-Hao-Bo Deng

Guangdong Academy of Agricultural Sciences

Qihang Wu

Guangzhou University

Shi-Zhong Wang

Sun Yat-Sen University

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Considering that even contaminated soils are a potential resource for agricultural production, it is essential to develop a set of cropping systems to allow a safe and sustainable agriculture on contaminated lands while avoiding any transfer of toxic trace elements to the food chain. In this review, three main strategies, i.e., phytoexclusion, phytostabilization, and phytoextraction, are proposed to establish cropping systems for production of edible and non-edible plants, and for extraction of elements for industrial use. For safe production of food crops, the selection of low-accumulating plants/cultivars and the application of soil amendments are of vital importance. Phytostabilization using non-food energy and fiber plants can provide additional renewable energy sources and economic benefit with minimum cost of agricultural measures. Phytoextracting trace elements (e.g., As, Cd, Ni, and Zn) using hyperaccumulator species is more suitable for slightly and moderately polluted sites, and phytomining of Ni from serpentine soils has shown a great potential to extract Ni-containing bio-ores of economic interests. We conclude that appropriate combinations of soil types, plant species/cultivars, and agronomic practices can restrict trace metal transfer to the food chain and/or extract energy and metals of industrial use and allow safe agricultural activities.

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Pedosphere 22(4): 470–488, 2012

ISSN 1002-0160/CN 32-1315/P

2012 Soil Science Society of China

Published by Elsevier B.V. and Science Press

Designing Cropping Systems for Metal-Contaminated Sites: A Review∗1

TANG Ye-Tao1,2,3, DENG Teng-Hao-Bo1, WU Qi-Hang1, WANG Shi-Zhong1,2, QIU Rong-Liang1,2, WEI Ze-Bin4,

GUO Xiao-Fang4, WU Qi-Tang4,LEIMei

5, CHEN Tong-Bin5, G. ECHEVARRIA3, T. STERCKEMAN

M. O. SIMONNOT6and J. L. MOREL

3,∗2

1School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275 (China)

2Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangzhou 510275 (China)

3INPL(ENSAIA)/INRA, Laboratoire Sols et Environnement, 2 Avenue de la Forˆet de Haye, BP 172, 54505 Vandoeuvre-l`es-Nancy

Cedex (France)

4College of Natural Resource and Environment, South China Agricultural University, Guangzhou 510642 (China)

5Center for Environmental Remediation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of

Sciences, Beijing 100101 (China)

6Laboratoire R´eactions et G´enie des Proc´ed´es (LRGP), Universit´e de Lorraine-CNRS (UPR 3349), 1 Rue Grandville BP20451, 54001

Nancy Cedex (France)

(Received February 4, 2012; revised May 10, 2012)

ABSTRACT

Considering that even contaminated soils are a potential resource for agricultural production, it is essential to develop a set of

cropping systems to allow a safe and sustainable agriculture on contaminated lands while avoiding any transfer of toxic trace elements

to the food chain. In this review, three main strategies, i.e., phytoexclusion, phytostabilization, and phytoextraction, are proposed

to establish cropping systems for production of edible and non-edible plants, and for extraction of elements for industrial use. For

safe production of food crops, the selection of low-accumulating plants/cultivars and the application of soil amendments are of vital

importance. Phytostabilization using non-food energy and ﬁber plants can provide additional renewable energy sources and economic

beneﬁt with minimum cost of agricultural measures. Phytoextracting trace elements (e.g., As, Cd, Ni, and Zn) using hyperaccumulator

species is more suitable for slightly and moderately polluted sites, and phytomining of Ni from serpentine soils has shown a great

potential to extract Ni-containing bio-ores of economic interests. We conclude that appropriate combinations of soil types, plant

species/cultivars, and agronomic practices can restrict trace metal transfer to the food chain and/or extract energy and metals of

industrial use and allow safe agricultural activities.

Key Words: agronomic practices, food safety, hyperaccumulator, phytoremediation, trace element

Citation: Tang, Y. T., Deng, T. H. B., Wu, Q. H., Wang, S. Z., Qiu, R. L., Wei, Z. B., Guo, X. F., Wu, Q. T., Lei, M., Chen, T. B.,

Echevarria, G., Sterckeman, T., Simonnot, M. O. and Morel, J. L. 2012. Designing cropping systems for metal-contaminated sites: A

review. Pedosphere. 22(4): 470–488.

INTRODUCTION

The scarcity of soil resources as human population

continuously increases will inevitably force farmers to

cultivate on contaminated areas. In the long run, this

issue will be of most importance for land contami-

nated with heavy metals (e.g., Cd, Hg, Ni, Pb, and

Zn) and other trace elements (e.g., As and Se), as re-

gard to their persistence in soils. Soil contamination

is a widespread phenomenon, and soil-to-plant trans-

fer and eﬀects of metals have been well documented

(e.g., Morel, 1997). It is now established that metals

can be phytotoxic, plants are unable to grow in some

circumstances (e.g., high metal concentration and low

pH), and the toxic metals can be transferred to edible

plant parts at rates suﬃcient to cause a threat to hu-

man health. Such phenomena have led governments to

ban food production in large surface areas of land con-

sidered too contaminated regarding the risks for popu-

lation health unless decontamination procedures are

previously conducted.

Hot spots of metal pollution can generally be mana-

ged and remediated by means of heavy technologies

based on excavation, treatment, and subsequent reuse

of treated materials for landscaping and soil construc-

tion (S´er´eet al., 2008; Simonnot and Croze, 2008), but

such technologies are neither economically nor environ-

mentally feasible for large surface areas. In general,

∗1Supported by the NSFC-Guangdong Joint Foundation of China (No. U0833004) and the National Natural Science Foundation of

China (No. 40901151).

∗2Corresponding author. E-mail: jean-louis.morel@ensaia.inpl-nancy.fr.

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 471

vast sites are abandoned and under strong surveillance

regarding their possible negative impacts on human

health and environmental targets, such as water bod-

ies, air, and ecosystems. In principle, they are seldom

used for economical purposes, and even less for food

production.

However, in densely populated countries such as

China, some contaminated land is already exploited

for food production to compensate the loss of agri-

cultural surface due to urbanization. It has been re-

ported that 1/5 of agricultural land of the country is

currently contaminated (Chen, 2007), making agricul-

ture on metal-contaminated soils obligatory. Similarly,

in other industrialized countries, such as Europe (e.g.,

France), land has to be removed from traditional agri-

cultural use (i.e., food production) as a result of con-

tamination with metals (e.g., deposition from metal

smelters and mine sites and wastewater spreading over

long period of time). Moreover, with the increasing de-

mand for safer food, which will undoubtedly reduce

the quality standards, more care will be required for a

large portion of land with soil-to-plant transfer risks of

toxicants.

Therefore, there is no other alternative besides de-

veloping new agricultural scenarios suitable for such

environments, to allow safe and economically valuable

agriculture on areas that are currently considered inap-

propriate and toxic. The new strategies to be develo-

ped should be based on the designing of suitable agro-

ecological and even forest systems combining biomass

production and management of contaminants in or-

der to minimize the risks for adjacent environments,

crops, and human beings, and provide regular revenue

to the farmers. There are two main options: i) remo-

ving pollutants according to economically and techni-

cally reasonable means, applicable to large surfaces,

while using land for valuable plant production and ii)

managing contaminants, e.g., growing plants with spe-

ciﬁc methods to minimize transfer from soil to edible

plant part and avoid dispersion of contaminants in the

environment; in the latter case, designed cropping sys-

tems have to focus on production quality rather than

on soil remediation. Of course, in both options, plants

(e.g., species, variety, and agricultural practices) are

part of the challenge, and phytoremediation appears

as a relevant remediation process. Phytoremediation,

a concept which has emerged in the 1990s (Salt et al.,

1994), after having been suggested earlier (Chaney,

1983), covers a set of soil treatments based on pro-

cesses induced by plant roots on pollutants (i.e.,sta-

bilization, extraction, and degradation). Following the

study of Baker et al. (1991), which opened the way

for phytoextraction of Zn using hyperaccumulators,

much work has been conducted at the international

level demonstrating the potential of accumulating and

hyperaccumulating plants for the remediation of metal-

contaminated soils. Removal of metals by plants sig-

niﬁcantly reduces the available pool (Chardot et al.,

2005), such as that for Ni (Echevarria et al., 2006), Cd

(G´erard et al., 2001), and Zn (Sinaj et al., 2004). Ano-

ther application of phytoremediation is stabilization

through the reduction of solubility and transport (solu-

ble, colloidal) of pollutants as a result of rhizosphere

interactions (e.g.,Morelet al., 1986) and root activity.

Phytostabilization is generally combined with amend-

ment additions to increase metal immobilization (Rut-

tens et al., 2010), and allows growth of edible plants.

However, phytoremediation is only part of the solu-

tion, and there is a great need for comprehensive agro-

nomic approaches to deal with contaminated soils. As

a remediation process, phytoremediation can only be

considered as an element to be included in sustainable

production systems adapted to contaminated environ-

ments.

Considering that even contaminated soils are a po-

tential resource for plant production, it is necessary to

propose sets of agricultural scenarios and recommenda-

tions to permit plant growth and avoid dissemination

of toxic elements, and to extract them for further eco-

nomical use. In this perspective, this paper is a contri-

bution to the future development of cropping systems

which would allow a safe and regular agricultural ac-

tivity on contaminated soils while avoiding any trans-

fer of metals to the food chain. From the knowledge

acquired in the management of contaminated land, we

have examined three main situations where agriculture

has to be conducted on metal contaminated soil: i) pro-

duction of edible plants, ii) production of non-edible

plants of industrial interests, and iii) extraction of el-

ements for industrial use. Then, we have attempted

to suggest appropriate cropping systems which would

require more scientiﬁc and technologic attention in the

near future.

CROPPING SYSTEMS FOR PRODUCTION OF

EDIBLE PLANTS

General principles and goals

There is increasing concern that cultivation of edi-

ble plants on contaminated soil can lead to the up-

take and accumulation of heavy metals in the edible

parts with their concentrations exceeding statutory or

advisory limits (e.g., legal limit set by FAO/WHO)

(Zhuang et al., 2009; Nabulo et al., 2010; Singh et al.,

472 Y. T. TANG et al.

2010; Luo et al., 2011). It is therefore imperative to

develop suitable strategies to restrict the metal accu-

mulation in such crops and its further transfer to the

food chain. The main principle is to use phytoexclu-

sion strategy, which is involved in the selection and

breeding of low-accumulating cultivars, reduction of

bioavailable metals in the soil, and restriction of their

potential uptake and translocation by plants.

Cereals

In the past decades, there have been reports that

the uptake and translocation of heavy metal pollutants

in plants varies greatly, not only among plant species

but also among cultivars within the same species

(John, 1973; Morishita et al., 1987; Wu et al., 1994,

1999; Cieslinski et al., 1996; Yu et al., 2006; Wu et al.,

2007a). Recently, there have been studies of signiﬁcant

diﬀerences in the uptake of heavy metals among cul-

tivars of rice (Oryza sativa L.), maize (Zea mays L.),

wheat (Triticum aestivum L.), and soybeans (Glycine

max L.). Studies on the genotypic diﬀerences in heavy

metal concentrations in cereal crops are summarized in

Table I.

The selection of rice cultivars to minimize heavy

metal accumulation by the plant has been extensively

studied. Wu et al. (1999) evaluated 20 cultivars of rice

in South China on a contaminated soil and their re-

sults showed that the grain Cd concentrations ranged

from 0.48 to 1.17 mg kg−1. The main reason causing

the diﬀerences was that the low-accumulating cultivar

exhibited a much lower Cd translocation rate to grains

than the high accumulating cultivar. In recent years,

most studies have been conducted on the molecular

mechanism of the low-accumulating rice cultivar. A

novel mapping population consisting of 39 chromosome

segment substitution lines (CSSLs) was used to locate

the putative quantitative trait loci (QTLs) for Cd con-

centration in brown rice (Ishikawa et al., 2005a). Xue

et al. (2009) found that 3 QTLs on chromosomes 6 and

7 controlled root and shoot Cd concentrations. Ueno

et al. (2010) reported that the gene (OsHMA3) was

responsible for low Cd accumulation in rice.

Heavy metal concentrations have also been shown

to vary among wheat cultivars (Oliver et al., 1995;

Cieslinski et al., 1996; Zhang et al., 2002a; Gao et

al., 2011). Erdman and Moul (1982) evaluated 7 cul-

tivars of durum wheat and reported that their grain

Cd, Cu, and Zn concentrations ranged from 0.13 to

0.25 mg kg−1with an average of 0.22 mg kg−1.Gaoet

al. (2011) also found that the wheat cultivars showed

signiﬁcant genotypic diﬀerences in grain concentrations

of Cd and Zn. Greger and Lofstedt (2004) observed

that diﬀerences among the cultivars in the ability to ac-

cumulate Cd in grain were related to variations in the

translocation from root to shoot and within the shoot,

rather than to diﬀerences in root uptake. Similar trends

were observed by Harris and Taylor (2004). Clarke et

al. (1997) found that grain Cd concentrations were

largely controlled by a single gene. The low-Cd wheat

cultivar Strongﬁeld (Clarke et al., 2005) was released in

2004 and is now sown on more than 25% of the durum

area in Canada (Grant et al., 2008).

Guo et al. (2010) observed that the grain Cd, Pb,

Zn, and Cu concentrations in sweet corn cultivars were

higher than those of normal corn cultivars. Analysis of

17 varieties of soybean showed that the soybean variety

En-b0-1-2 was the low-Cd cultivar in both ﬁeld and pot

experiments (Arao et al., 2003b). Low-accumulating

maize and soybean cultivars appeared to retain more

heavy metals in the root and translocate less to the

grain than high-accumulating ones (Arao et al., 2003b;

Ishikawa et al., 2005b; Guo et al., 2010).

Vegetables

Similar to cereal crops, vegetables have a variety

of capacities in accumulating heavy metals among dif-

ferent types of species. The leafy vegetables tend to

accumulate higher amounts of heavy metals in edible

TAB L E I

Studies on genotypic diﬀerences in heavy metal concentrations in cereal crops

Crop References

Rice (Oryza sativa L.) Morishita et al., 1987; Wu et al., 1994, 1999; Arao and Ae, 2003a; Liu et al., 2003b, 2005a, 2007a;

Li et al., 2005b; Yu et al., 2006, 2008; Fu et al., 2008; Shi et al., 2009

Wheat (Triticum aestivum L.) Erdman and Moul, 1982; Oliver et al., 1995; Cieslinski et al., 1996; Clarke et al., 1997; Zhang et

al., 2000, 2002a; Greger and Lofstedt, 2004; Harris and Taylor, 2004; Clarke et al., 2005; Gao et al.,

2011

Maize (Zea may L.) Florijn and Beusichem, 1993; Gao et al., 1995; Kurz et al., 1999; Samake et al., 2003; Tudoreanu

and Phillips, 2004; Guo et al., 2010

Soybean (Glycine max L.) Reddy and Dunn, 1986; Arao et al., 2003b; Ishikawa et al., 2005b

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 473

parts than fruit or even root vegetables (Zheng et al.,

2007; Wang et al., 2009a; Zhuang et al., 2009; Khan

et al., 2010), although this is not always the case. The

high metal accumulation in leafy vegetables is regarded

as a result of their high rates of transpiration and

translocation of metals, particularly Cd (Khan et al.,

2010). In addition, leafy vegetables are fairly suscepti-

ble to physical contamination by soil dust and splash

because of their high foliar surface area (Zhuang et

al., 2009). Accumulation of Pb and Cr in leafy vege-

tables resulting from aerial deposition is substantially

greater than that of Cd, Zn, Ni, and Cu, of which the

uptake occurs predominantly via the roots and subse-

quent transport to the edible shoot tissues. This high-

lights the importance of mulching vegetable gardens to

reduce exogenous metal contaminants on leaves (Na-

bulo et al., 2010).

Heavy metal accumulation may also diﬀer greatly

within cultivars of an individual species when grown

on the same soil. Wide variation of metal accumulation

within cultivars has been documented in potato (Dun-

bar et al., 2003), carrot, pea (Alexander et al., 2006),

asparagus bean (Zhu et al., 2007), and several leafy

vegetables (Wang et al., 2007b, 2009a). Alexander et

al. (2006) tested ﬁve cultivars of six common vegetables

and found that carrot and pea cultivars exhibited sig-

niﬁcant intra-species diﬀerences in Cd and Cu. Wang et

al. (2009a) observed that there were large genetic vari-

ances in water spinach Cd concentration, ranging from

0.593 to 1.824 mg kg−1among 30 tested cultivars when

grown on Cd-treated soil. Among them, six cultivars

were identiﬁed as pollution-safe cultivars and the pre-

ferential sequestration of Cd in root and cell wall frag-

ment was one possible mechanism leading to low Cd ac-

cumulation. Using suppression subtractive hybridiza-

tion analysis, Huang et al. (2009) found tremendous

diﬀerences in Cd-induced gene expression in two water

spinach cultivars with contrasting Cd-accumulating ca-

pacity, suggesting that Cd-accumulating ability of this

species is a genotype-dependent and inherited trait.

Orchards

One of the most common elevated trace metal con-

taminants in fruit orchard soils is Cu. The long-term

use of Cu-based fungicides has resulted in elevated ac-

cumulation of Cu in soils of vineyard and apple or-

chard, typically ranging from 200 to 500 mg kg−1

(Chopin et al., 2008). The values are over ten times

higher than the typical background Cu concentrations

in soils (5–30 mg kg−1) (Wightwick et al., 2010).

There are increasing concerns of Cu availability

in orchard soils and its subsequent accumulation in

grapevines (Mirlean et al., 2005; Lai et al., 2010). The

adverse eﬀects of Cu accumulation in apple orchard

and vineyard soils on enzymatic activity, microbial

community, and soil invertebrates have also been em-

phasized (Wang et al., 2009b; Zhou et al., 2011). In

some vineyard sites of central Taiwan, high accumu-

lation of Cu up to 86 mg kg−1in grape berries was

reported, far exceeding the maximum residue level of

Cu in wine grapes (20 mg kg−1) proposed by the Eu-

ropean Regulation (Lai et al., 2010). In contrast, much

lower Cu content (4.5 mg kg−1) was observed in berries

grown in a calcareous contaminated Champagne vine-

yard area, France (Chopin et al., 2008). In fact, many

studies have demonstrated that the availability of Cu is

dominated by soil factors such as pH, cation exchange

capacity (CEC), clay content, and organic matter con-

tent. Cu availability in soil is generally lowest in neu-

tral soils and increases with increasing soil acidity and

alkalinity (Wightwick et al., 2010). This may have im-

portant implications in considering strategies (e.g., soil

pH management) to reduce Cd availability and toxi-

city in vineyards. On the other hand, several studies

suggested that organic carbon is responsible for a sub-

stantial retention of Cu mainly by increasing CEC, and

thus application of compost is another feasible option

to reduce Cu mobility in vineyard soils (Lai et al., 2010;

Wightwick et al., 2010). From the long run, it is wise

to restrict or even stop the use of Cu-based fungicides,

and develop environmentally safer alternatives to Cu-

based fungicides, which have been banned in some Eu-

ropean countries like the Netherlands (Lai et al., 2010).

Chemical immobilization of heavy metals in soil

In-situ chemical immobilization is a cost-eﬀective

way to reduce metal concentrations in plants through

the addition of chemical amendments in soil, which

may provide a solution through the formation of low

solubility and/or precipitation of minerals (Basta and

McGowen, 2004). Kumpiene et al. (2008) reviewed the

published papers during 2000–2005 on immobilization

of As, Cr, Cu, Pb, and Zn in soils.

Research on chemical immobilization of heavy me-

tals has included alkaline substances, phosphate- and

silicon-based materials, adsorption agents, and organic

matters. Alkaline substances, such as lime, have been

used in traditional agricultural practice to raise soil pH

levels for plant growth (Simon, 2005). The addition of

alkaline amendments reduced heavy metal solubility

in soil by increasing soil pH and formed insoluble com-

pounds (Maddox and Soileau, 1991; Chen et al., 2000;

Khan and Jones, 2009). One of the disadvantages of

liming is that the gradual reduction of the liming agent

474 Y. T. TANG et al.

over time due to dissolution and leaching, which can

be accelerated by acid deposition, may have a poten-

tial risk that needed to be considered prior to long-term

phytoexclusion practices (Ruttens et al., 2010).

Silicon (Si) is not considered to be an essential

mineral element for plants, but has been shown to

ameliorate the deleterious eﬀects of metals on plants

grown on contaminated soils (Liang et al., 2005, 2007;

da Cunha and do Nascimento, 2009). Silicon applied

in agriculture came mainly from by-products of ﬂy-ash

(Dwivedi et al., 2007), steel sludge, furnace slag (Chen

et al., 2000), and Si chemicals (Shi et al., 2005; Li et

al., 2009c; Gu et al., 2011). Liu et al. (2009) reported

that foliar application of silica sols signiﬁcantly in-

creased the dry weight of rice grains and shoots grown

on Cd-contaminated soils, whereas the Cd concentra-

tion apparently decreased in the grains and shoots. The

mechanism of Si foliar application to alleviate the to-

xicity and accumulation of Cd in rice grains may be

related to the co-precipitation of Cd with Si in stems

(Gu et al., 2011), and probable Cd sequestration in the

shoot cell walls (Liu et al., 2009).

Phosphate-based materials added to contamina-

ted soils reduced the Pb mobility by ionic excha-

nge and precipitation of pyromorphite-type minerals,

Pb5(PO4)3X, where X = F, Cl, or OH (Kumpiene

et al., 2008). The phosphate-based materials include

phosphate rock (Zwonitzer et al., 2003; Cao et al.,

2004; Brown et al., 2005), diammonium phosphate

(Basta and McGowen, 2004; Chen et al., 2007; Khan

and Jones, 2009), phosphate-based salts (Ownby et al.,

2005; Simon, 2005; Li et al., 2008), and phosphoric acid

(Cao et al., 2003).

Adsorption agents such as zeolites, iron and/or

manganese oxides, and clay minerals have also been

widely studied because of their high cation exchange

capacity and high speciﬁc surface. In a pot experi-

ment, natural zeolites decreased the available part

of Pb and restricted Pb uptake by rape (Li et al.,

2009a). Among 15 metal ions investigated, addition of

vermiculite signiﬁcantly reduced the uptake of various

metal pollutants by lettuce and spinach (Malandrino

et al., 2011). A similar reduction eﬀect on Cd and Zn

accumulation in radish and Japanese mustard spinach

wasreportedwhen5%lherzolitewasappliedinacon-

taminated soil (Kashem et al., 2010).

Organic matters such as peat, animal excrement,

and composts can also eﬀectively be used in metal sta-

bilization. Li et al. (2008) reported that pig manure

and peat could increase grain yields and decrease Cu

and Cd concentrations in grain.

CROPPING SYSTEMS FOR PRODUCTION OF

NON-EDIBLE PLANTS

Energy crops

The technology development and utilization of phy-

toremediation using tolerant energy crops can pro-

vide additional economic beneﬁts (Meers et al., 2005,

2010). These crop cultivars are cultivated on metal-

contaminated soils for energy production purposes,

and the sustainable development of resilient energy

plants has turned into a new trend in the developed

and developing countries.

Industrial non-food crops have been used for both

remediation of contaminated land and renewable ene-

rgy sources (Meers et al., 2007). Canola (Brassica na-

pus var. Hyola) plants grown under adverse soil condi-

tions in the west side of the San Joaquin Valley (SJV)

accumulated Se in various plant organs including seeds.

The Se-enriched economically viable phyto-products of

canola such as seed oil have been used as biofuel ad-

ditive and organic fertilizer (Ba˜nuelos, 2006; Ba˜nuelos

et al., 2010).

A number of studies have indicated that many ene-

rgy plants (e.g., sunﬂower, willow, and poplar) have

high tolerance to heavy metals such as Cu, Cd, Cr, and

Zn (Lin et al., 2003; Lun´aˇckov´aet al., 2003; Rosselli

et al., 2003). In addition, soybean (Glycine max) oil,

palm (Trachycarpus fortunei) oil, and coconut (Cocos

nucifera) oil have been considered as possible substi-

tutes for fossil diesel (Agarwal, 2007). Hence, metal-

tolerant industrial and energy crops are suitable can-

didates for long-term ﬁeld remediation and sustainable

economic development. This process could be of par-

ticular importance in countries with increasingly less

arable land, such as China and India, due to the rapid

expansion of population and urbanization.

Jatropha curcas L. (Euphorbiaceae) is a perennial

oil-yielding plant cultivated in the tropical and sub-

tropical regions of the world. It has been widely used

for energy plantations and wasteland reclamation due

to the ability to tolerate extreme environmental condi-

tions such as drought, non-fertile, and heavily polluted

soils. Based on the accumulation of diﬀerent trace ele-

ments (Cu, Cr, Mn, Ni, and Zn) and nutrients (Ca,

K, Mg, Na, and P) in J. curcas grown in the vicinity

of a mica belt, it could be used for phytostabilization

of mining areas (Nagaraju and Karimnlla, 2002). Re-

cent studies have mainly focused on the improvement

of growth performance and metal tolerance of J. curcas

grown on metal-contaminated calcareous soils with the

amendments of organic wastes (biosludge and dairy

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 475

sludge) and a biofertilizer (Azotobacter chroococcum)

(Juwarkar et al., 2008; Kumar et al., 2008; Yadav et

al., 2009, 2010).

J. curcas can also grow well on the acid mine

drainage irrigated soils (pH ≥3.78) with addition of ≤

1% limestone in extremely acidic soils (Li et al., 2009d;

Wu et al., 2011). The growth performance of J. cur-

cas was enhanced at 0.50% of lime addition due to the

increase of soil pH and the decrease of phytoavailable

Al (about 95%), Zn (about 75%), and Cu (about 65%)

in soil. The high ability to tolerate Al was suggested

to relate to cell wall binding and the organic acids se-

creted by the roots of J. curcas (Wu et al., 2011). Based

on the inherent tolerance ability of J. curcas in exis-

ting adverse environmental conditions, it could be used

as a suitable candidate for phytostabilization in acid

mine tailings. Eﬀective stabilization of liming is an ad-

ditional possible practice to improve the soil quality.

Fiber crops

Bast ﬁber crops are widely grown in China and

throughout the world. The characteristics of ﬁber crops

include fast growth, strong adaptability, large biomass,

and high economic value. The bast ﬁbers are widely

applied in textiles, adsorbents, and building materi-

als (Liu et al., 2003a; Hasfalina et al., 2010). These

non-wood ﬁbers were also proved to be suitable for pa-

permaking (Saikia et al., 1997; Ververis et al., 2004).

Recent attention has been given to ﬁber crops as a

potential plant for heavy metal-contaminated soils due

to its tolerance (Angelova et al., 2004; Ho et al., 2008;

Yang et al., 2010). Hemp (Cannabis sativa) could grow

under 17 mg kg−1Cd in soil and 1 mmol L−1Cu in cul-

ture solution without showing any phytotoxicity symp-

toms (Citterio et al., 2003; Arru et al., 2004). Through

a large-scale ﬁeld investigation and a hydroponic cul-

ture experiment, ramie (Boehmeria nivea) has been

revealed to possess a certain degree of constitutional

metal tolerance to As, Cd, Pb, and Zn (Yang et al.,

2010).

However, due to the presence of toxic metals, high

soil acidity, and poor physical properties with deﬁ-

ciency of nutrients in the vicinity of mine tailings (Pich-

tel and Salt, 1998; Ernst, 2005), ﬁber crops are hard to

grow in these contaminated areas. Therefore, revege-

tation process should combine with application of soil

amendments, especially those that can neutralize soil

pH and enhance nutrition. A 3-year ﬁeld experiment on

a stripmine land showed that the yield of kenaf (Hibis-

cus cannabinus) increased with sewage sludge applica-

tion (Carlson et al., 1982). Similar results were also

found in a pot trial by applying chicken manure to a

Pb-contaminated soil (Ho et al., 2008).

In another ﬁeld trial conducted in Shangba Vil-

lage, Guangdong, China, where the farmland soil was

highly polluted by acid mine drainage from upstream

mine tailings, the ameliorative eﬀects of lime, dolomite,

ﬂy ash, and compost were tested (Table II) (Huang,

2009). The contaminated soil was characterized by its

low pH (3.36) and high concentrations of heavy me-

tals (1 500, 10, 660, and 480 mg kg−1of Pb, Cd, Cu,

and Zn, respectively) (unpublished data). The soil pH

was adjusted to 7–8 by amendment application. The

yield of kenaf shoots could reach 20 t ha−1or above

(Fig. 1) (Zou, 2008), which is similar to those on nor-

mal soils, indicating a successful and sustainable mode

of reclaiming the acid mine soils by using kenaf in com-

bination with soil amelioration. Besides, low levels of

heavy metals were detected in kenaf ﬁbers. Meanwhile,

it was suggested that heavy metals had no signiﬁcant

negative eﬀects on ﬁber quantity and quality (Linger

et al., 2002; Wang et al., 2008). A highly contaminated

soil is always considered to be a wasteland. Howe-

ver, with a certain amendment applied into the soil,

ﬁber crops could grow healthily and rapidly. There-

fore, these crops are good candidates to cultivate on

highly contaminated soils for revegetation as well as

economic purposes.

Though the heavy metals in ﬁbers may not easily

enter the food chain and do harm to human beings di-

TAB L E I I

Eﬀects of diﬀerent amendment treatments on yields and agricultural and economic characteristics of kenaf (Huang, 2009)

Treatment Agronomic trait Biomass

Yield Stem diameter Stem height Bast ﬁber Stem core

tha

−1cm gplant

−1

Lime (0.6%) 22.0aba) 4.4a 308a 24.7a 63.0a

Dolomite (5%) 40.5b 6.2b 374a 47.9b 129.0b

Fly ash (5%) 30.7ab 5.9ab 358a 37.1ab 93.3ab

Lime (0.6%) + compost (5%) 35.0ab 5.4ab 356a 40.2ab 110.0ab

Lime (0.6%) + ﬂy ash (5%) 20.1a 5.6ab 351a 36.9ab 94.4ab

a)Means followed by the same letter(s) in a column are not signiﬁcantly diﬀerent at P<0.05.

476 Y. T. TANG et al.

Fig. 1 A ﬁeld trial of acid mine contaminated soil amendment in Shangba Village, Guangdong, China: (a) before growth of kenaf

and (b) after growth of kenaf (Zou, 2008).

rectly, a minimum amount of metals is expected in

these industrial raw materials. So, more attention

should be paid to amendment selection and soil mana-

gement practices to achieve the best crop yield and

least potential hazard.

CROPPING SYSTEMS FOR EXTRACTION OF

ELEMENTS FOR INDUSTRIAL USE

Phytoextraction of Cd, Ni and Zn: perspectives for phy-

tomining and soil remediation

General principles and goals. Nickel is the most

accumulated metal among hyperaccumulator plants.

Approximately 390 plant species have been reported

worldwide (Verbruggen et al., 2009) to hyperaccumu-

late Ni in their shoot tissues (i.e., Ni concentrations of

above 1 000 mg kg−1) and most of them easily reach 1%

Ni in their leaf tissues when growing on soils with suﬃ-

cient Ni availability (Massoura et al., 2004; Chardot et

al., 2005). Hyperaccumulation of Cd and Zn occurs to

be less than that of Ni (Peer et al., 2006; Verbruggen

et al., 2009). Also, only a few plant species are able

to take up both metals at high levels; these plants be-

long mainly to the family Brassicaceae (several species

of the Thlaspi/Noccaea genus and Arabidopsis hallerii)

as well as the species Sedum alfredii (Yang et al.,

2004). The co-hyperaccumulation is highly important

because most of the Cd-contaminated sites also display

high concentrations of Zn as these two metals are of-

ten present together in mineral ores and in industrial

wastes and by-products. Metal-rich soils and mainly

ultramaﬁc soils (i.e., serpentine soils) are widespread

over diﬀerent areas of the world including the Alps,

the Balkans, Turkey, New Caledonia, Cuba, Australia,

and many other regions. These soils are a major prob-

lem for the development of agriculture due to extreme

nutrient deﬁciency and toxicity of trace metals. The re-

covery of such metals from soils with hyperaccumulator

plant crops as an alternative to traditional agriculture

is a challenge for the rural development of these areas

as well as for the local mining and metallurgical indus-

try (Bani et al., 2007). Very often, ultramaﬁc soils are

too poor in metal contents for viable traditional mining

operations; phytomining, i.e., recovery of metal hyper-

accumulated in aboveground plant parts, proves to be

proﬁtable in these soils and becomes a true alterna-

tive to classical crops (Bani et al., 2007; Chaney et al.,

2007). Also, the prices of some metals (e.g., Ni, Co, and

Tl) have dramatically increased for the past ﬁve years

although a noticeable breakdown occurred during the

2009 crisis. During 2010, the prices of metals went up

again due to increasing demand of Asian industries; at

the time this text was written, the price of Ni at the

London Metal Exchange was USD $ 26 per kg. This

alone justiﬁes their mining from naturally rich soils or

their recycling when remediating metal-contaminated

soils. Industrial brownﬁeld and mining sites are also of-

ten contaminated with trace metals (Cd, Co, Cr, Cu,

Ni, and Zn), representing a major environmental con-

cern (De Kimpe and Morel, 2000). In the case of Cd

and Zn, the main objective of remediation is often re-

moval of the metal fractions that present a risk in co-

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 477

ntaminated soils. Removal of total contents of metals in

contaminated soils is often impossible thermodynami-

cally speaking but has long been considered as an is-

sue by stakeholders (Schwartz et al., 2003; Keller and

Hammer, 2004). Now, it is commonly accepted that

the main goal of phytoextraction of Cd and Zn is to

deal with keeping low the bioavailable fractions of these

metals to prevent excessive uptake in following crops

or leaching to groundwater. However, the recovery of

metals in the produced biomass could be a way of re-

ducing the overall costs of contaminated soil treatment,

especially considering the expected increases in Cd and

Zn market values in the forthcoming years.

Phytomining of Ni: agronomic perspectives. Se-

veral ﬁeld trials and research programs have led to

a better understanding of phytomining and proposed

several sets of agronomic practices to end-users (Li et

al., 2003; Bani et al., 2007; Chaney et al., 2007). It

is quite easy to grow Ni-hyperaccumulator plants in

pot conditions on a wide array of soils and treatments

(Robinson et al., 1999) and signiﬁcant amounts of Ni

can be recovered after three months with Ni concentra-

tions in shoots reaching more than 3% and depletion of

total soil Ni reaching almost 5% (Kukier et al., 2004;

Massoura et al., 2004; Chardot et al., 2005). However,

ﬁeld-scale phytomining requires approaches that inte-

grated species selection and breeding, phenology and

cropping calendar, fertilization practices, and pest con-

trol (Chaney et al., 2007). Two approaches have been

developed so far: one intensively designed that includes

all aspects of mechanized agriculture available in deve-

loped countries (Li et al., 2003; Chaney et al., 2007)

and the other extensively designed that is adapted

to ultramaﬁc areas in the world where no modern

cropping tools are available (Bani et al., 2007; Bani,

2009). The latter needs the same scientiﬁc basic know-

ledge to optimize agronomic options. Some studies

on the phenology of Alyssum murale showed that the

curves of Ca, Mg, and Ni uptake during plant growth

and development deﬁned the mid-ﬂowering stage as the

best stage for harvesting with the highest Ni concen-

trations and the lowest Ca concentrations in shoots

(Bani, 2009). Chaney’s group led a breeding program

with various species of Alyssum (Li et al., 2003), among

which A. murale from eastern Albania proved to be

one of the best candidates (Bani et al., 2009). The se-

lected strains were able to accumulate 3% Ni in the

shoots (including stems) as compared to 2% as a best

value in the wild (Bani et al., 2009), with reasonably

increased yields (up to 20 t ha−1in ﬁeld conditions)

and a better retention of leaves that are the richest

parts in the plant (Chaney et al., 2007). Optimization

of soil fertility concerns mainly nitrogen (Bani et al.,

2007). A. murale is very eﬃcient in taking up phospho-

rus (P) and soil P fertility is seldom a limiting factor

(Shallari et al., 2001; Bani et al., 2007). However, N

fertilization is seriously required and it was possible

to limit N inputs to 100 kg N ha−1by fractioning its

application (Chaney et al., 2007; Bani, 2009). Since

most Ni hyperaccumulators take up large amounts of

Ca from Ca-deﬁcient serpentine soils, it is necessary to

maintain Ca fertility of such soils at a reasonable level

(Kukier et al., 2004; Chaney et al., 2007).

Phytoextraction of Cd and Zn with hyperaccumula-

tor plants at the ﬁeld scale. Several teams in the

past twenty years have carried out experiments on

Cd and Zn phytoextraction by hyperaccumulators at

the ﬁeld scale and conﬁrmed what had been studied

at the lab scale although the adaptation of species

such as Noccaea caerulescens to the ﬁeld is not so

easy (Schwartz et al., 2003; Keller and Hammer, 2004;

Chaney et al., 2005, 2007). To date, most studies have

shown that although N. caerulescens can be used to

clean up soils slightly or moderately contaminated by

Cd and Zn (Ernst, 2005; McGrath et al., 2006), the

technology usually needs a long period (e.g.,10years)

for cleanup due to the limited biomass production

of hyperaccumulator species used (Koopmans et al.,

2008). Also, the phytoextraction duration can be un-

derestimated since the bioavailable metal pools in soil

decrease during phytoextraction, which leads to a de-

crease of metal uptake by plants and lower metal re-

moval rates (Koopmans et al., 2008). Thus, phytoex-

traction appears possible for Ni and As, but for Cd and

Zn, the strategy is still far from large-scale practice

(Van Nevel et al., 2007). One of the keys for successful

phytoextraction operations based on N. caerulescens

requires an increased biomass production.

Metal recovery in hyperaccumulator biomass. Ni

is used in a wide variety of alloys and superalloys but

the largest needs concern the production of stainless

steel. For this reason, there is a wide variety of pro-

cesses for Ni recovery that mainly depend on the type

of and the concentrations of Ni in ores. Currently,

about twenty processes are known, among which 6

are signiﬁcantly used at the industrial scale, e.g.,

pyrometallurgy (INCO and Falconbridge, Canada) and

hydrometallurgy (Eramet-SLN, France). Some scien-

tists have shown that pyrometallurgical processes can

be used to produce pure Ni from hyperaccumulator

plant residues (Boominathan et al., 2004). This process

is however diﬃcult to promote in developed countries

because of the strict environmental regulations. Other

scientists promote co-incineration of hyperaccumula-

478 Y. T. TANG et al.

tor plants along with municipal wastes (Keller et al.,

2005). This also causes problems in terms of social ac-

ceptability and diﬃculty to recover metals that may

escape with ﬂy ashes. These ashes would then need a

special treatment as dangerous wastes. One alterna-

tive to pyrometallurgy to valorize phytoextracted me-

tals could be a hydrometallurgical process that better

responds to clean technology standards (Barbaroux et

al., 2009, 2011, 2012). Hydrometallurgy consists in a

set of techniques used for a long time (Habashi et al.,

2005). The yearly world production of Ni (over one

million tons) is mainly based on pyrometallurgy but

hydrometallurgy is also used because of the possibili-

ties it oﬀers for the elaboration of end products and for

the recovery of metals in complex systems. Therefore,

it is essential to continue development and adaptation

of hydrometallurgical methods, in particular lixiviation

methods, lixiviate puriﬁcation, and production routes

of end products, in order to valorize metals present in

various environmental materials. Biomass produced by

phytomining is a substantial resource (i.e., 2% Ni), for

which a speciﬁc separation process should be develo-

ped.

Phytoextraction of As

Several plant species have been reported as As hy-

peraccumulators, primarily represented by terrestrial

Pteris species (Ma et al., 2001; Chen et al., 2002b;

Wang et al., 2007a) and aquatic seaweeds (Nguyen et

al., 2011). Some angiosperms, e.g., Brassicaceae Isatis

cappadocica (Karimi et al., 2009) and Hesperis per-

sica (Karimi et al., 2010), and ferns, e.g., marsh fern

(Anderson et al., 2010), have also been reported as

As hyperaccumulators. Pteris vittata has the merits of

large biomass, high As concentration, and wide distri-

bution; thus, it has been widely used in phytoextrac-

tion projects (Chen et al., 2007; Ebbs et al., 2009).

P. vittata has a wide distribution. Diverse habi-

tats result in diﬀerent genotypes. Although all ecotypes

of P. vittata could hyperaccumulate As, the ability of

hyperaccumulating As was very variable. The above-

ground As concentration of P. vittata ranged from 643

to 3 009 mg kg−1(Cai et al., 2007). It means that using

diﬀerent genotypes in phytoremediation projects could

lead to several times of variations in the remediation

eﬃciency. Therefore, diﬀerences in As accumulation by

P. vittata genotypes were investigated and the 3–4 fold

As accumulation diﬀerences were conﬁrmed (Wang et

al., 2002; Zhao et al., 2002; Wu et al., 2009). It was

found that some P. vittata ecotypes also had huge po-

tentials in phytoextracting other toxic trace elements,

e.g., Zn, Cd, Cr, and Hg (Anet al., 2006; Su et al.,

2008b; Xiao et al., 2008; Roccotiello et al., 2010; Feng

et al., 2011; Kalve et al., 2011). The reasons behind

such ecotypic variations have not been identiﬁed yet,

but these research results clearly showed the necessity

to select appropriate genotypes according to the situ-

ation of contaminated ﬁelds.

Besides plant selection, complementary approaches

to optimize plant growth and increase As concentration

in P. vittata have been adopted. The uses of fertilizers

(phosphate and nitrogen) and mycorrhizal fungi have

received focused attention and both were able to in-

crease the remediation eﬃciency (Chen et al., 2002a;

Liu et al., 2005c; Wei and Chen, 2006; Huang et al.,

2007; Liao et al., 2007; Leung et al., 2010; Muthuku-

mar and Bagyaraj, 2010; Xiong et al., 2010). The ef-

fect of phosphate fertilizers is still unclear (Huang et

al., 2007; Santos et al., 2010).

In addition, the optimization of environmental fac-

tors including soil properties, seedling age, and har-

vesting regimes has also been reported (Gonzaga et

al., 2007; Wan et al., 2010; Xu et al., 2010; Natarajan

et al., 2011). Younger seedlings have been found to ex-

tract As more quickly, but whether we should adopt

young plants or apply more frequent harvest regimes

still depends on the balance between larger biomass

and higher concentrations.

A ﬁeld experiment conducted showed that P. vit-

tata can achieve maximum extraction eﬃciency by

mowing 3 times a year, and the stubble height had

a great impact on the P. vittata growth and extraction

eﬃciency: a stubble height of 7.5 cm beneﬁted the re-

generation of P. vittata and the extraction eﬃciency of

arsenic (Li et al., 2005a).

In the plant tissues of arsenic hyperaccumulators

(Pteris species), inorganic arsenic species arsenate

(As(V)) and arsenite (As(III)) account for more than

95% of the total arsenic, while organic species have

been detected as minor compounds (Ma et al., 2001;

Tu et al., 2002, 2004; Zhang et al., 2002b; Mathews et

al., 2010). Regardless of As(III) or As(V) supplied, As

exists predominantly as As(V)–O in roots while mainly

as As(III)–O in the rhizomes and fronds (Huang et al.,

2008; Mathews et al., 2010). Arsenite was ﬁrstly oxi-

dized in the growing medium and then further oxidized

in the roots of P. vittata (Huang et al., 2004; Mat-

hews et al., 2010). Arsenate was mainly reduced in the

rhizomes (68%–71% as As(III)) and pinnae (>90%

as As(III)), and limitedly reduced in the roots (7%–

8% as As(III)) (Huang et al., 2004; Mathews et al.,

2010). Monomethylarsonic acid (MMA) can be methy-

lated to dimethylarsinic acid (DMA), while DMA can-

not be demethylated to MMA. Both MMA and DMA

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 479

can be oxidized to arsenate (As(V)) and arsenite

(As(III)) (Chen et al., 2004). Arsenic transformation

mechanism has not yet been clearly explored and still

leaves much to be resolved.

Phytoextraction faces the challenge of safe dis-

posal of large quantities of contaminant-rich biomass

after harvesting from contaminated sites (Cao et al.,

2010). Incineration was considered to be suitable for

hyperaccumulators after harvest. During incineration

of P. vittata containing high As content (1 170 mg

kg−1), about 24% of total As was emitted at 800 ◦C,

and 62.5% of the total emitted As was volatilized below

400 ◦C. Simultaneously, below 400 ◦C, As(V) reduced

to As(III) (Yan et al., 2008). The ash weight was about

4.4%–7.7% of the dried weight and the concentration of

heavy metals presented regular variations in diﬀerent

stages of incineration. As concentration in the bottom

ash was lower than that in the ﬂy ash.

CO-CROPPING FOR REDUCING HEAVY METAL

CONTENTS IN CROPS

Co-cropping of a hyperaccumulator (N. caerule-

scens) with a non-accumulator (Thlaspi arvense)in-

creased the growth of the non-accumulator and re-

duced its Zn uptake, while in contrast, increased

Zn uptake of the hyperaccumulator (Whiting et al.,

2001). Comparing with monoculture, intercropping de-

creased the Cd content in the aboveground parts of al-

falfa (a normal crop) by 57.1%, while increased the Cd

content in the aboveground parts of Brassica juncea (a

high Cd accumulator) by 14.5% for the soils with Cd

contents in the range of 0.37–5.37 mg kg−1(Li et al.,

2009e). The Cd contents in the aboveground parts of

alfalfa under monoculture and intercropping were 0.21

and 0.09 mg kg−1, respectively, neither of them being

over the feed safety standard (Li et al., 2009e). High

Cd-accumulating varieties of oilseed rape could reduce

the Cd uptake of co-cropped cabbage, but the Cd con-

centration in cabbage was still high (Liu et al., 2007b;

Su et al., 2008a). Therefore, a low-metal crop is needed

to produce safe agricultural products on contaminated

agricultural lands in association with a hyperaccumu-

lator. Growing a metal hyperaccumulator plant S. al-

fredii alongside a low metal-accumulating cultivar of

maize was introduced to simultaneously phytoextract

heavy metals from contaminated sewage sludge and to

produce an agricultural crop (Liu et al., 2005b). Re-

sults showed that this co-planting system eﬀectively

removed heavy metals from the sewage sludge by the

hyperaccumulator while the harvested corn grains or

Alocasia tubers were conformed to the Chinese stan-

dard for animal feeds (Liu et al., 2005a; Wu et al.,

2007b).

However, the beneﬁcial eﬀect on the co-cropped

normal crop was not always observed from the co-

cropping with a hyperaccumulator. Combined crop-

ping of N. caerulescens and Hordeum vulgare, though

caused a decrease in Zn concentration in barley bio-

mass, had a signiﬁcant increase in Cd accumula-

tion (Gove et al., 2002). Similar results were also

obtained by Jiang et al. (2010). The average Cd

concentration in ryegrass shoots was increased by

co-cropped N. caerulescens, but the Zn concentra-

tion and total uptake by ryegrass were decreased

by co-cropping with N. caerulescens compared with

mono-cropping or co-cropping with T. arvense (non-

hyperaccumulator). These observations suggest that

the hyperaccumulator competes for Zn against the co-

planted crop, but not always true for Cd, probably be-

cause the hyperaccumulator does not need Cd for the

physiological functioning of the plant and may mobilize

too much Cd which may be absorbed by the co-planted

crop.

Co-cropping of two normal crops may also alter the

availability of metals. Wheat/rice intercropping could

reduce Cd uptake by wheat and rice in shoots and re-

duce Cd concentration in the wheat grain; however, Cd

concentration in rice grain was increased, compare to

that in the monocultured plant (Wu et al., 2003). In

the intercropping system of Cunninghamia lanceolata

in tea gardens, the concentrations of Pb, Mn, Cu, and

Zn in the tea leaves were signiﬁcantly lower than those

in the mono-cropping one, indicating that intercrop-

ping C. lanceolata in tea gardens can improve the quali-

ty of the tea (Xue and Fei, 2006).

Continued agricultural production of safe animal

feeds or energy crops on contaminated soils is necessary

considering the limited arable land in China and time

required for phytoremediating metal-contaminated

soils. Co-cropping or intercropping may alter condi-

tions in shared rhizosphere and thereby aﬀect the avail-

ability of selected metals to neighboring plants. There-

fore, it is possible that planting some low-metal crops

in association with hyperaccumulators or other ap-

propriate plants may allow agricultural production on

heavy metal-contaminated soils.

CO-CROPPING FOR ENHANCING PHYTOEX-

TRACTION

Co-cropping N. caerulescens with T. arvense in-

creased Zn uptake by the hyperaccumulator (Whiting

et al., 2001). Combined cropping of N. caerulescens

and Hordeum vulgare caused a higher concentration

of heavy metals (Cd, Pb, and Zn) in the biomass of

480 Y. T. TANG et al.

the hyperaccumulator N. caerulescens (Gove et al.,

2002). It may indicate a potential approach to increase

the remediation eﬃciency of metal-contaminated soils

in a natural way.

A co-planting system, comprised of a Zn and Cd

hyperaccumulator (S. alfredii) and a low-accumulating

crop (Z. mays), was established in a rice ﬁeld that was

historically irrigated with water aﬀected by Pb and Zn

mining activities (Wu et al., 2007c). The co-planting

system enhanced not only the removal of heavy metals

from the contaminated soils but could also produce

safe corn for animal feed, allowing farmers to continue

their agricultural activities. The co-cropping of a Cd

hyperaccumulator Brassica napus with B. parachinen-

sis or Zea mays increased the Cd concentration and

accumulation in the shoot of the hyperaccumulator

plant (Selvam and Wong, 2009). Co-cropping system

could combine with chemical enhancement, including

chelator-enhanced phytoextraction (Wu et al., 2007c)

and chemical washing (Huang et al., 2010), to further

increase the phytoextraction eﬃciency.

For the non-hyperaccumulators, Li et al. (2009b)

studied the eﬀect of 7 intercrops on Cd uptake by

maize for naturally enhancing the phytoremediation

with high biomass plants and the results showed that

legumes substantially increased Cd uptake by maize.

However, maize is not a hyperaccumulator so that its

phytoextraction eﬃciency is low, and the disposal of

the produced biomass with metal contents generally

too low to be recovered should be considered.

In a pot experiment conducted to study the in-

teraction mechanisms between the roots of two co-

cropped plants with the corn roots separated from S.

alfredii with a mesh barrier, co-cropping decreased pH

of the sludge solution, increased dissolved organic car-

bon (DOC), and resulted in higher Zn/Cd concentra-

tion than the S. alfredii mono-cropping, which caused

more Zn/Cd transported to the S. alfredii side and then

enhanced the uptake of the heavy metals by the hyper-

accumulator (Hei et al., 2007). The concentrations of

Cu, Pb, Zn, Cd, and Fe in the shoots of peas grown in

a mixed culture with barley in pots were 1.5, 1.8, 1.4,

1.4, and 1.3 times higher than those of the monocul-

ture (Luo et al., 2008). The root exudates from barley

in the mixed culture system played an important role

in the process of solubilizing metals in soil and facili-

tating the uptake of metals by peas.

The enhancing eﬀect on the phytoextraction de-

pends on plant species in co-cropping. For example,

intercropping of Salix caprea with the hyperaccumula-

tor Arabidopsis halleri did not enhance total Zn and Cd

extraction compared to single plantings (Wieshammer

et al., 2007), which is potentially due to competition

for water or nutrients and possibly metal sequestration

into plants. Athyrium yokoscens, a fern that hyperac-

cumulates Zn and Cd, is often accompanied by another

Zn and Cd-hyperaccumulating plant, Arabis ﬂagellosa;

a mixed planting of two plants of each species did not

largely changed the levels of Zn and Cd accumulated

by these two plants (Chen et al., 2009), which may be

related to competition for metals, and indicated that

it would be better to intercrop plants that hyperaccu-

mulate diﬀerent metals.

CONCLUSIONS

This review presents a broad summary and evalu-

ation of cropping systems that are available for trace

element-contaminated sites. Three major cropping sys-

tems are identiﬁed, each of which targets on one of

the following crop production: edible plants, non-edible

plants, and bio-ores for industrial use (Fig. 2). The pri-

mary strategies include phytoexclusion, phytostabiliza-

tion, and phytoextraction/phytomining. Each strategy

has beneﬁts and limitations, depending on the remedial

goals targeted and on-site and species-speciﬁc factors.

For safe production of edible food crops such as

cereals and vegetables, further research is needed to

select low-accumulating species/cultivars by means of

agronomic and genetic breeding. Chemical amend-

ments (e.g., alkaline agents, adsorption agents, and

fertilizers) should be optimized according to their eﬃ-

ciency of metal immobilization and the economic feasi-

bility. In this case, the designed cropping system needs

to be evaluated mainly by production quality rather

than soil remediation.

At contaminated sites with harsh soil conditions

(e.g., acidity, low fertility, and multiple metals), crop-

ping industrial non-food energy and ﬁber plants will

likely be preferred. However, more attention should

be paid to amendment selection and soil management

practices to achieve a best crop yield and least poten-

tial hazard. On the other hand, for large-scale sites

with low to moderate levels of trace elements (e.g.,

As, Cd, Ni, and Zn), a plant-based phytoextraction

will be a possible option for decontamination of met-

als and/or extraction of metals with high price (e.g.,

Ni). However, the technology can in some cases be

time-consuming and it is anyway limited to the soil

depth prospected by roots of hyperaccumulators. Thus,

high-biomass hyperaccumulating species should be se-

lected, and further research is required for better un-

CROPPING SYSTEMS FOR METAL-CONTAMINATED SITES 481

482 Y. T. TANG et al.

derstanding the mechanisms involved in metal hyper-

accumulation. Further, biomass produced by phytomi-

ning is a substantial resource (i.e., 2% Ni), for which

a speciﬁc separation process should be developed.

Co-cropping two plant species with contrasting

metal-accumulating abilities could improve phytore-

mediation eﬃciency and remediate metal-contami-

nated soils in a naturally enhanced way. The intera-

ction mechanisms between the two plants deserve fur-

ther investigation and the combination ratios of the

two plants are warranted to be optimized.

In summary, the majority of these cropping sys-

tems are still far from maturity at present, but they

have shown the potential for a safe and regular agri-

culture on large-scale sites contaminated with trace

elements in a cost-eﬀective manner. With appropriate

combination of soil types, plant species/cultivars, and

agronomic managements, toxic metals into the food

chain will be restricted and the potential beneﬁts of-

fered by these cropping systems can be substantial in

the long run.

ACKNOWLEDGEMENT

Tang Ye-Tao gratefully acknowledges the grant

from the China Scholarship Council (CSC).

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Zwonitzer, J., Pierzynski, G. M. and Hettiarachchi, G. M. 2003.

Eﬀects of phosphorus additions on lead, cadmium, and zinc

bioavailabilities in a metal-contaminated soil. Water Air

Soil Pollut.143: 193–209.

Effect of Cd toxicity on root morphology, ultrastructure, Cd uptake and accumulation of wheat under intercropping with Solanum nigrum L

Article

Full-text available

Jun 2023

In order to evaluate the effect of intercropping of the hyperaccumulator, Solanum nigrum L. and wheat on the absorption and accumulation of cadmium (Cd) in wheat. The experiment was conducted with three replicates, which conducted on four Cd concentrations (0, 20, 40, 60 μmol L−1) in the Hoagland solution and using two planting patterns [monoculture wheat (MW), intercropping wheat and Solanum nigrum L. (IW，IS)]. The results showed that the addition of Cd in the solutions reduced the total root length by 19.08–55.98%, total root area by 12.35–44.48%, and total root volume by 16.01–46.00% of wheat plants. Intercropping with Solanum nigrum L. significantly reduced Cd contents by 28.3–47.2% and Cd accumulations by 10.08–32.43% in the roots of wheat. Transmission electron microscope (TEM) revealed that the root-tip cells of the monoculture wheat treated with Cd exhibited swollen spheres of intracellular mitochondria, disorderly arranged inner ridges of mitochondria, some damaged mitochondrial membranes, and deformed nuclear membranes. Many dense electron particles in the form of Cd were deposited in the cell gap, and the cell nucleus became smaller or even disappeared. Under the same Cd concentrations, root-tip cells of intercropped wheat showed much less density of electron particles, starch granules, and the damage to the nucleus and nuclear membrane by Cd.These results indicated that intercropping with Solanum nigrum L. reduced the Cd toxicity to wheat roots and decreased Cd uptake and accumulation in both the shoots and roots of the wheat.

Phytoremediation of Heavy-Metal-Contaminated Soils: Capacity of Amaranth Plants to Extract Cadmium from Nutrient-Poor, Acidic Substrates

Article

Full-text available

May 2023

Soil pollution is a threat to food security and ecological and human health. Cd is one of the most common pollutants in agricultural soil and, due its human toxicity, one of the most hazardous. Amaranth is a documented hyperaccumulator of Cd and other pollutants, and it is commonly grown in Asia and South America. A considerable amount of amaranth is grown in suboptimal conditions, including nutrient-poor acidic soils. The objective of this experimental study was to examine the capacity of Amaranthus hypochondriacus to extract Cd from a nutrient-poor, acidic substrate that was spiked with different concentrations of Cd (2 and 20 mg kg−1 dw) during a period of 180 days. The plants grown in the substrate that was spiked with 20 mg Cd kg−1 dw did not develop into mature plants, but the plants grown in substrate that was spiked with 2 mg Cd kg−1 dw extracted a significant amount of Cd from the substrate by accumulating it into the above-ground biomass. The Cd levels varied from 113 to 176 mg kg−1 in the stems at the four measuring points, and from 64 to 94 mg kg−1 in the leaves. The concentrations in the plants increased with time and reached a maximal concentration of 176 ± 45 mg kg−1 dw for stems and 94 ± 41 mg kg−1 dw for leaves after 180 days. The mean bioaccumulation factor in the plants was 86 ± 15 after 90 days, 72 ± 12 after 120 days, 105 ± 37 after 150 days, and 99 ± 31 after 180 days, which confirms the previously reported capacity of Amaranthus hypochondriacus to hyperaccumulate Cd. Amaranthus hypochondriacus may, thus, be used to improve ecological and human health by remediating moderately Cd-polluted soils, even in nutrient-poor acidic soils.

Contaminated soil remediation with Nano-FeS loaded lignin hydrogel: A novel strategy to produce safe rice grains while reducing cadmium in paddy field

Article

Mar 2024
J HAZARD MATER

Cash/valuable crop production on polluted land

Chapter

Jan 2024

The agricultural extensification on polluted lands

Chapter

Jan 2024

Edible crop production on polluted lands for biofortification

Chapter

Jan 2024

Designer cropping systems in phytoremediation programs

Chapter

Jan 2024

Patterns of accumulation and baseline values for metals in agricultural soils from a copper mining region in southern Peru

Article

Full-text available

Nov 2023

Dataset of metals and metalloids in food crops and soils sampled across the mining region of Moquegua in Peru

Article

Full-text available

Jul 2023

In recent years, there has been an increase in interest in the accumulation of heavy metals and metal(loid)s (HMM) in areas where agriculture and mining exist side by side. As a contribution to this body of knowledge, we report the first dataset into HMM concentrations in food crops and agricultural soils in Moquegua, which is a typical mining region and contains one of Peru’s largest copper deposits. Thanks to its geographic diversity, samples were taken in different agroecological regions at altitudes between 9 and 3,934 m. For food crops, 31 elements were measured using inductively coupled plasma mass spectrometry and atomic absorption spectrometry. For soils, 23 elements were measured using inductively coupled plasma optical emission spectrometry. Thus, the dataset includes a total of 13,828 observations from 341 sampling sites. We hope that this dataset will facilitate a wide range of agricultural and food safety studies, as well as serving as a reference for monitoring changes in pollution over time or comparing HMM levels with other farmlands influenced by mining activities.

An integrated remediation approach using combinations of biochar, Rhizobium leguminosarum, and Vigna radiata for immobilizing and dissipating cadmium contaminants from the soil–mustard plant system

Article

Full-text available

Mar 2023

Cadmium (Cd) contamination of soils is an environmental concern, as cadmium harms food crops and can therefore impact human health. The use of combinations of biochar (seeded with Rhizobium leguminosarum) and Vigna radiata (as an intercrop) has the potential to reduce the mobilization of Cd from soil via mustard plants (Brassica juncea). Mustard plants are grown as a food and oil production crop that is consumed worldwide. However, this plant has the property of hyperaccumulation; thus, it bioaccumulates Cd in its tissues, which in turn, if eaten, can become part of the human food chain. Hence, reducing Cd bioaccumulation in mustard plants is crucial to making these plants a reliable and safe source of food for consumption. To improve soil sorption capacity and immobilization efficiency, biochar (in the form of wheat husk) was mixed with R. leguminosarum and intercropped (using V. radiata) with mustard plants for further investigation. Sampling was performed at an early growth stage (i.e., at 30 days) and at maturity (i.e., at 60 days) to determine the impact of Cd on a plant’s morphophysiological attributes. Data were analyzed in two ways: first by analysis of variance (ANOVA) and then by the post hoc Tukey’s honestly significant difference (HSD) test. The statistical analysis concluded that combinations effectively improved plant traits by 65%–90% in the early growth stage and by 70%–90% in the maturity stage. The T6 treatment combination [i.e., biochar + R. leguminosarum + V. radiata (BC + RL + VR)] provided the most effective results in terms of growth, biomass, pod yield, and pigmentation content. In addition, this combination reduced the translocation of Cd in mustard plants by 70%–95%. The combination of BC + RL + VR effectively reduced Cd contamination of mustard tissue and provided a suitable growing environment for the plants. A post-harvesting soil analysis using X-ray diffraction (XRD) found that Cd was undetectable in soil. This provides clear confirmation that these approaches can lead to Cd soil remediation. Moreover, this study provided insight into the responses of different morphophysiological attributes of mustard plants to Cd stress and could aid in developing Cd stress tolerance in mustard plants.

Bioavailability of trace elements to terrestrial plants

Article

Jan 1997

Jean-Louis Morel

The influence of interspecific interactions on Cd uptake by rice and wheat intercropping

Article

Jan 2003

Effects of intercropping Cunninghamia lanceolata in tea garden on contents and distribution of heavy metals in soil and tea leaves

Article

Oct 2006

Effects of intercropping Cunninghamia lancealata in tea gardens on contents and distribution of heavy metals in the soil an tea leaves were analyzed, through comparison study of a mono-cropping tea garden and an intercropping tea garden. Results show (1) contents of Pb, Ni, Mn and Zn decreased in the intercropping tea plantation, and the absorption capacity of Cunninghamia lanceolata varied from element to element, displaying an decreasing order of Mn > Ni > Pb > Zn; (2) concentrations of the heavy metals in the tea leaves of the intercropping tea garden were significantly lower than in the mono-cropping one. So intercropping of Cunninghamia lanceolata in tea gardens can significantly decrease contents of Pb, Ni, Mn and Zn and improve quality of the tea.

Effect of crop cultivars and chemical fertilizers on the cadmium accumulation in plants

Article

Jan 1994

Procédés de traitement physique et chimique des sols pollues

Article

Aug 2015

Losartan arrests aortic root enlargement in Marfan syndrome independent of hemodynamic effects

Article

Oct 2005

Haline lacustrine biohermal reservoir characters in Block Da 81-4 of the Yidong Oil Field, East China

Article

Aug 2003

Phytoremediation of arsenic-contaminated soil in China

Article

Jan 2007

Genotypic difference in growth and As accumulation in Pteris vittata

Article

Jan 2007

Immobilization and re-vegetation of heavy metal polluted soils in Dabao Mountain, Guangdong Province by amendments

Article

Sep 2008

The effects of chemical amendments on heavy metals immobilization of contaminated soils (agro-discard soil and acid mine-tailing soil) were determined. The effectiveness of limestone, zeolite and fly ash to reduce the metal availability to pea on the two types of heavily contaminated soils was evaluated. The growth and uptake of heavy metals by pea in amended soils were studied in pot experiments under greenhouse conditions. The application of both limestone and fly ash increased the soil pH. All tested amendments decreased the metal availability in both the soils and decreased the heavy metals uptake by pea compared with the unamended control. Pea failed to establish in acid mine tailing control and the zeolite treatments, but grew in agro-discard control and other treatments. The biomass of pea increased with a factor 2.4 (soil amended with limestone), 2.6 (soil amended with zeolite), 2.9 (soil amended with zeolite and limestone), 2.7 (soil amended with fly ash) and 2.9 (soil amended with fly ash and limestone) with respected to unamended soil. Fly ash appeared more efficient than other amendments in reducing plant metal concentrations, and the mixture of amendments showed more efficient than they were applied alone. Cd, Cu, Pb and Zn concentration in pea under fly ash plus limestone treatment decreased by 94.6%, 69.3%, 80.6% and 87.3%, respectively, compared with the control. Soil chemical treatment improved the performance of crops by increasing soil pH, releasing nutrient elements to soils, and reducing bioavailability of metals in the soils. The results suggest that fly ash and limestone can be used to remediate heavily contaminated acid soils to allow re-vegetation.

Designing Cropping Systems for Metal-Contaminated Sites: A Review

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