Journal of Hazardous Materials 266 (2014) 141–166

Contents lists available at ScienceDirect

Journal of Hazardous Materials

journal homepage: www.elsevier.com/locate/jhazmat

Review

Remediation of heavy metal(loid)s contaminated soils – To mobilize

or to immobilize?
Nanthi Bolan a,b,∗ , Anitha Kunhikrishnan c , Ramya Thangarajan a,b , Jurate Kumpiene d ,
Jinhee Park e , Tomoyuki Makino f , Mary Beth Kirkham g , Kirk Scheckel h
a
Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, Australia
b
Cooperative Research Centre for Contamination Assessment and Remediation of the Environment, Adelaide, Australia
c
Chemical Safety Division, Department of Agro-Food Safety, National Academy of Agricultural Science, Suwon-si, Gyeonggi-do, Republic of Korea
d
Waste Science and Technology, Department of Civil, Environmental and Natural Resources Engineering, Luleå University of Technology, Luleå SE-97187,
Sweden
e
Centre for Mined Land Rehabilitation, University of Queensland, St Lucia, Australia
f
Soil Environmental Division, National Institute for Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki, Japan
g
Department of Agronomy, 2004 Throckmorton Plant Sciences Center, Kansas State University, Manhattan, KS, USA
h
National Risk Management Research Laboratory, U.S. Environmental Protection Agency, 5995 Center Hill Avenue, Cincinnati, OH 45224, USA

h i g h l i g h t s g r a p h i c a l a b s t r a c t

• Amendments used for remediation

of contaminated soils influence
metal(loid) bioavailability.
• Case studies demonstrating the
application of mobilization and
immobilization techniques.
• Techniques to monitor the long-term
stability of immobilized metal(loid)s.
• Environmental implications of mobi-
lization and immobilization tech-
niques.

a r t i c l e i n f o a b s t r a c t

Article history: Unlike organic contaminants, metal(loid)s do not undergo microbial or chemical degradation and persist
Received 24 July 2013 for a long time after their introduction. Bioavailability of metal(loid)s plays a vital role in the reme-
Received in revised form 6 December 2013 diation of contaminated soils. In this review, the remediation of heavy metal(loid) contaminated soils
Accepted 12 December 2013
through manipulating their bioavailability using a range of soil amendments will be presented. Mobi-
Available online 21 December 2013
lizing amendments such as chelating and desorbing agents increase the bioavailability and mobility of
metal(loid)s. Immobilizing amendments such of precipitating agents and sorbent materials decrease the
Keywords:
bioavailabilty and mobility of metal(loid)s. Mobilizing agents can be used to enhance the removal of
Metals
Metalloids
heavy metal(loid)s though plant uptake and soil washing. Immobilizing agents can be used to reduce the
Bioavailability transfer to metal(loid)s to food chain via plant uptake and leaching to groundwater. One of the major
Mobility limitations of mobilizing technique is susceptibility to leaching of the mobilized heavy metal(loid)s in
Soil amendments the absence of active plant uptake. Similarly, in the case of the immobilization technique the long-term
stability of the immobilized heavy metal(loid)s needs to be monitored.
© 2013 Elsevier B.V. All rights reserved.

∗ Corresponding author at: CERAR, Building X, UniSA, University Boulevard, Mawson Lakes, SA 5095, Australia. Tel.: +61 8 8302 6218; fax: +61 8 8302 3124.
E-mail address: Nanthi.Bolan@unisa.edu.au (N. Bolan).

0304-3894/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jhazmat.2013.12.018
142 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142
2. Sources of heavy metal(loid)s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
2.1. Geogenic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
2.2. Anthropogenic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
3. Dynamics of heavy metal(loid)s in soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
3.1. Sorption/desorption process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
3.2. Precipitation/dissolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144
3.3. Oxidation/reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144
3.4. Methylation/demethylation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
4. Approaches and indicators of bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
4.1. Approaches to bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
4.2. Indicators of bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
5. Soil amendments for remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
5.1. Mobilization of soil contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
5.1.1. Desorbing agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
5.1.2. Chelating agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
5.1.3. Organic amendments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
5.1.4. Fertilizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149
5.1.5. Saline waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
5.1.6. Microbial mobilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
5.2. Immobilization (stabilization) of soil contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
5.2.1. Phosphate compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
5.2.2. Liming materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152
5.2.3. Organic composts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152
5.2.4. Metal oxides . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153
5.2.5. Biochar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153
6. Case studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154
6.1. Case study 1: soil washing for cadmium contaminated paddy soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154
6.2. Case study 2: immobilization of copper and lead in mine spoil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155
6.3. Case study 3: immobilization of arsenic in soil contaminated with wood impregnation chemicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156
6.4. Case study 4: immobilization of lead in smelter residue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156
7. Environmental implications of (im)mobilization techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157
7.1. Leaching of contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157
7.2. Long-term stability of immobilized metal(loid)s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
8. Summary and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160

1. Introduction metal(loid)s such as As, Cu, and Pb in soils resulting from excessive
use of fungicides and herbicides that are rich in these metal(loid)s
Indiscriminate waste disposal practices have led to significant [5].
build up in soils of a wide range of metal(loid)s, such as arsenic (As), Unlike organic contaminants, metal(loid)s do not undergo
cadmium (Cd), chromium (Cr), copper (Cu), mercury (Hg), lead (Pb), microbial or chemical degradation, and the total concentration of
selenium (Se), and zinc (Zn). Entry of soil-borne metal(loid)s into these metal(loid)s persist for a long time after their introduction
the food chain depends on the amount and source of metal(loid) in soils [6]. With greater public awareness of the implications of
input, the properties of the soil, the rate and magnitude of uptake contaminated soils on human and animal health there has been
by plants, and the extent of absorption by animals [1]. Health increasing interest amongst the scientific community in the devel-
authorities in many parts of the world are becoming increasingly opment of technologies to remediate contaminated sites. This is
concerned about the effects of heavy metal(loid)s on environmen- especially necessary since traditional methods of soil removal and
tal and human health. Historically, heavy metal(loid) toxicity to replacement of clean soil is often cost prohibitive. For diffuse dis-
human health received attention primarily as a result of series of tribution of metal(loid)s, remediation options generally include
widespread poisoning. For example, the hundreds of tragic cases of amelioration of soils to minimize the metal(loid) bioavailability.
human poisoning of Minamata Bay in Japan (Minamata disease) in Bioavailability can be minimized through chemical and biological
the late 1950s were believed to have occurred from the ingestion immobilization of metal(loid)s using a range of inorganic com-
of fish containing methyl mercuric compounds probably derived pounds, such as lime and phosphate (P) compounds, and organic
through biomethylation of mercuric salts by aquatic organisms [2]. compounds, such as ‘exceptional quality’ biosolids [7]. The more
More recently high concentrations of heavy metal(loid)s, such localized metal(loid) contamination found in urban environments
as As, Cd, Cu, Pb, and Zn in soils have often been reported in num- is remediated by metal(loid) mobilization processes that include
ber of countries. For example, significant adverse impacts of As on phytoextraction and chemical washing. Removal of metal(loid)s
human health have been recorded in Bangladesh, India, and China through phytoextraction process and the subsequent recovery of
and it is claimed that millions of people are potentially at risk from the metal(loid)s or their safe disposal are attracting research and
As poisoning [3]. Similarly, Cd accumulation in the offal of graz- commercial interests [8]. However, when it is not possible to
ing animals in New Zealand and Australia made it unsuitable for remove the metal(loid)s from the contaminated sites by phytoex-
human consumption and affected access of meat products to over- traction, other viable options, such as in situ immobilization (e.g.,
seas markets [4]. Similarly, there have been concerns about urban phytostabilization) should be considered as an integral part of risk
development of horticultural sites which contained toxic levels of management (Fig. 1). Both phytoextraction and phytostabilization
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Fig. 1. Schematic diagram illustrating the link between (im)mobilization, bioavail-
ability and remediation of heavy metal(loid)s.
precesses are part of phytoremediation technique employed to
manage contaminated soils.
An overview of the sources of some of the common heavy
metal(loid)s input to soils, their interactions and bioavailability
in soils, and the remediation of metal(loid) contaminated soils
through manipulating their bioavailability using a range of mobi-
lizing and immobilizing soil amendments will be presented in this
review.
2. Sources of heavy metal(loid)s
In terrestrial ecosystems, the soil is the main repository of chem-
ical contaminants. Likewise in aquatic systems, the sediment serves
as the ultimate sink for these chemicals. Heavy metal(loid)s reach
the soil environment through both pedogenic and anthropogenic
processes. Most heavy metal(loid)s occur naturally in soil parent
materials, chiefly in forms that are not readily bioavailable for
plant uptake. Unlike pedogenic inputs, heavy metal(loid)s added
through anthropogenic activities typically have a high bioavail-
ability [9–11]. Anthropogenic activities, primarily associated with
industrial processes, manufacturing, the disposal of domestic and
industrial waste materials, and the application of P fertilizers are
the major source of metal(loid) enrichment in soils [1,12–14].
2.1. Geogenic
Most of the heavy metal(loid)s occur in nature, the major source
of which is weathering of soil parent materials including igneous
and sedimentary rocks, and coal. The majority of As is derived from
geogenic origin. For example, coal is estimated to release 45,000
tons of As annually, while human activities release approximately
50,000 tons [15,16]. The As content of igneous rocks varies widely
(up to 100 mg/kg); the average content is 2–3 mg/kg. Sedimentary
rocks also vary in their As content, from small amounts in lime-
stone and sandstone up to 15,000 mg/kg in some manganese ores
[17]. Although the anthropogenic As source is increasingly becom-
ing important, the recent episode of extensive As-contamination
of ground waters in many countries including Bangladesh, India,
China, and Mexico is of geological origin, transported by rivers from
sedimentary rocks in the Himalayas over tens of thousands of years
[16,18–20].
Similarly, seleniferous soils found in the areas of Se-rich rocks,
such as black shales, carbonaceous limestones, carbonaceous
cherts, mudstones, and seleniferous coal are a major source of Se
input to soil. Also, irrigation of Se-rich ground water had shown
to contaminate irrigation drain water and surface waters in the
San Joaquin Valley, California (United States), and in Punjab, India
[21,22]. Volcanic and geological activities mobilize natural Hg from
143
deep reservoirs in the earth to the atmosphere. Annual emission of
Hg from global mercuriferous belts, the zone along plate tectonic
including western North America, central Europe, and southern
China was estimated up to 500 Mg/year [23,24].
2.2. Anthropogenic
Anthropogenic activities, primarily associated with indus-
trial processes, manufacturing and the disposal of domestic and
industrial waste materials are the major source of metal(loid)
enrichment in soils. Atmospheric pollution from Pb-based petrol
was a major issue in many countries where there was no constraint
on the usage of leaded gasoline [25]. While biosolids is the major
source of metal(loid) inputs in Europe and North America, P fer-
tilizers are considered to be the major source of heavy metal(loid)
input, especially Cd, in Australia and New Zealand [4,12,26,27].
Phosphate compounds contain a range of metal(loid)s [4,12,28].
Cadmium contamination of agricultural soils is of particular con-
cern because it reaches the food chain through regular use of
Cd-containing P fertilizers. The Cd in most P fertilizers originates
mainly from the phosphate rocks (PRs) used for manufacturing
P fertilizers. Although many countries have formulated threshold
levels for Cd and other heavy metal(loid) accumulation in soils
due to the use of municipal biosolids, such limits have not been
established from fertilizer use.
Large quantities of Cu are used in agriculture, horticulture, and
animal industries as a trace element, in many formulations of Cu
containing fungicides, such as copper oxychloride and ‘Bordeaux’
mixture, and as a growth promoter in piggery and poultry units
[29,30]. Accumulation of Cu in agricultural soils resulting from con-
tinuous use of Cu fungicides and biosolids application has been
reported in many countries [31–34]. One of the major consequences
of excessive accumulation of Cu in soils is its toxicity to plants
and microbial communities, for instance, formation of bare sterile
patches in orchards [35,36].
Approximately 6400 and 1600 tons of tannery and timber
treatment effluents, respectively, are generated annually in New
Zealand, and these effluents are considered to be the major sources
of Cr contamination into aquatic and terrestrial environments [37].
Chromium is used as Cr(III) in the tannery industry and as Cr(VI)
in the timber treatment industry. Chromate is highly toxic and car-
cinogenic even when present in very low concentrations in water.
Large scale use of Cu–Cr–As (CCA) treated timber as fence post and
in vineyards can also result in the release of Cu, Cr, and As to soil
environment [38,39].
3. Dynamics of heavy metal(loid)s in soils
Metal(loid) ions can be retained in the soil by sorption, pre-
cipitation, and complexation reactions, and are removed from soil
through plant uptake, leaching, and volatilization (Fig. 2). Although
most metal(loid)s are not subject to volatilization losses, some
metal(loid)s such as As, Hg, and Se tend to form gaseous com-
pounds [16,40]. The fate of metal(loid)s in the soil environment
is dependent on both soil properties and environmental factors.
3.1. Sorption/desorption process
Retention of charged metal(loid) solute species by charged
surfaces of soil components is broadly grouped into specific
and non-specific retention [41,42]. In general terms, non-specific
adsorption is a process in which the charge on the ions balances
the charge on the soil particles through electrostatic attraction,
whereas specific adsorption involves chemical bond formation
between the ions in the solution and those in the soil surface
[43–45].
144 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Fig. 2. The interaction between adsorption reactions of metal(loid)s in soil and their
bioavailability.
Both soil properties and soil solution composition determine
the dynamic equilibrium between metal(loid)s in solution and the
soil solid phase. The concentration of metal(loid)s in soil solution
is influenced by the nature of both organic and inorganic ligand
ions, and soil pH through their influence on metal(loid) sorption
processes [46,47]. Two reasons have been given for the effect of
inorganic anions on the sorption of metal(loid) cations such as Pb
and Cd [48–51]. Hong et al. [48] indicated that inorganic anions
form ion pair complexes with metal(loid)s, thereby reducing their
sorption. Naidu et al. [51] indicated that the specific sorption of lig-
and anions is likely to increase the negative charge on soil particles,
thereby increasing the sorption of Cd.
The effect of pH values >6 in lowering free metal(loid) ion activ-
ities in soils has been attributed to the increase in pH-dependent
surface charge on oxides of Fe, Al, and Mn, chelation by organic
matter, or precipitation of metal(loid) hydroxides (e.g., Pb(OH)3 )
[52,53]. The activity of heavy metal(loid)s (e.g., Cd and Pb) in solu-
tion in naturally acidic soils is found to decrease with increasing pH
which is attributed to increasing CEC [54–57].
Other chemical interactions that contribute to metal(loid) reten-
tion by colloid particles include complexation reaction between
metal(loid)s and the inorganic and organic ligand ions. As might
be expected, the organic component of soil constituents has a high
affinity for heavy metal(loid) cations such as Cu, Cd, and Pb because
of the presence of ligands or groups that can form chelates with
metal(loid)s [47,58]. With increasing pH, the carboxyl, phenolic,
alcoholic, and carbonyl functional groups in soil organic matter
dissociate, thereby increasing the affinity of ligand ions for these
metal(loid) cations. The extent of metal(loid)–organic complex
formation, however, varies with a number of factors including tem-
perature, steric factors, and concentration. All these interactions
are controlled by solution pH and ionic strength, the nature of the
metal(loid) species, dominant cation, and inorganic and organic
ligands present in the soil solution.
3.2. Precipitation/dissolution
Precipitation appears to be the predominant process in high pH
soils and in the presence of anions such as SO4 2− , CO3 2− , OH− , and
HPO4 2− , and when the concentration of the heavy metal(loid) ion is
high [54,59,60]. Precipitation of metal(loid) phosphates/carbonates
is considered to be one of the mechanisms for the immobilization
of heavy metal(loid)s such as Cu and Pb, especially in substrates
containing high concentration of these metal(loid)s. For example,
McGowen et al. [61] noticed that P decreased the leaching of Cd, Pb,
and Zn. Activity-ratio diagrams indicated that diammonium phos-
phate decreased solution metal(loid) concentrations by forming
metal(loid)–P precipitates. Similarly, liming typically enhance the
retention of metal(loid)s [1]. For instance, Bolan and Thiyagarajan
[62] found increased retention of Cr(III) with lime-induced increase
in pH.
16
15
14
13
12
11
Bacterial sp.
10
9
8
7
6
5
4
3
2
1
0 100 200 300 400 500
µ M/hr)
As(III) oxidation rate (µ
Fig. 3. Arsenite oxidation potential of various bacterial strains: (1) herminiimonas
arsenicoxydans ULPAs1, (2) thermus aquaticus, (3) thermus thermophiles, (4)
agrobacterium albertimagni AOL15, (5) agrobacterium tumefaciens-5A, (6) Achro-
mobacter sp. GW1, (7) thermus aquaticus AO3C, (8) ochrobactrum tritici SCII24,
(9) Achromobacter sp. SY8, (10) Pseudomonas sp. TS44, (11) Alcaligenes sp. RS-19,
(12) Marinobacter santoriniensis NKSG1, (13) Pseudomonas arsenicoxydans VC-1, (14)
Bosea sp. AR-11, (15) SPB-24, (16) SPB-31 [79].
Co-precipitation of metal(loid)s especially in the presence of
iron oxyhydroxides has also been reported and often such interac-
tions lead to significant changes in the surface chemical properties
of the substrate. Lu et al. [63] confirmed that co-precipitation of
Pb(II) with ferric oxyhydroxides occurred at ∼pH 4 and is more effi-
cient than adsorption in removing Pb(II) from aqueous solutions
at similar sorbate/sorbent ratios and pH. Arsenate (As(V)) sorp-
tion onto ferrihydrite, and Ni(II) and Cr(III) sorption onto hydrous
iron oxides showed that co-precipitation was more efficient pro-
cess than sorption for metal(loid) removal from aqueous solutions.
Violante et al. [64] noticed that As(V) was desorbed by P from a
ferrihydrite on which As(V) was added than from a Fe–As(V) co-
precipitate. The potential value of P and liming materials in the
remediation of metal(loid) contaminated soils is discussed below.
3.3. Oxidation/reduction
Metal(loid)s, including As, Cr, Hg, and Se, are most commonly
subjected to microbial oxidation/reduction reactions, thereby
influencing their speciation and mobility (Table 1). For example,
metals (e.g., Cu and Hg) generally are less soluble in their higher
oxidation state, whereas the solubility and mobility of metalloids
(e.g., As) depend on both the oxidation state and the ionic form [77].
The redox reactions are grouped into two categories, assimilatory
and dissimilatory [78]. In assimilatory reactions, the metal(loid)
(e.g., Se) substrate is involved in the metabolic functioning of the
organism by acting as terminal electron acceptor. In contrast, for
dissimilatory reactions the metal(loid) substrate has no known role
in the metabolic functioning of the species responsible for the reac-
tion, and indirectly initiates redox reactions.
Arsenic in soils and sediments can be oxidized to As(V) by bac-
teria [79,80] (Fig. 3). Since As(V) is strongly retained by inorganic
soil components, microbial oxidation results in the immobilization
of As. Under well drained conditions As would present as As(V),
whereas under reduced conditions, As(III) dominates in soils, but
elemental arsenic [As(0)] and arsine (H2 As) can also be present.
Oxidation of Cr(III) to Cr(VI) can enhance the mobilization and
bioavailability of Cr. It is primarily mediated abiotically through
oxidizing agents such as Mn(IV), and to a lesser extent by Fe(III),
whereas reduction of Cr(VI) to Cr(III) is mediated through both
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166 145

Table 1
Selected references on the effect of various soil amendments on the redox reactions of metal(loid)s in soils.

Metal(loid)s Soil amendments Observations References

Cr Cattle manure Enhanced the reduction of Cr(VI) to Cr(III). [65,66]

Cr Biosolid compost, Manures, spent mushroom Organic amendments increased DOC, which reduced Cr(VI) to Cr(III) in soils. [12]
Cr Composted cow manure Chromate leaching was reduced in soils in the presence of elevated organic matter [67]
because of reduction followed by retention on cation exchange sites or
precipitation.
Cr Zero valent iron Enhanced the reduction of Cr(VI) to Cr(III). [68]
Cr Colloidal zerovalent iron A majority of Cr(VI) was reduced at pH 5. [69]
Cr Mn oxide salts, birnessite and todorokite The amendments were equally capable of oxidizing Cr(III) to Cr(VI). [70]
As Iron oxide At lower redox, insoluble sulfides can be formed either with iron (AsFeS, [71]
arsenopyrite; at strongly reducing conditions) or without iron (As2 S3 , orpiment; at
moderately reducing conditions).
As Fe(III) and Mn(III) oxides Fe(III) and Mn(III) oxides oxidized As(III) to As(V) through electron transfer [16]
reaction.
As Goethite [␣-FeIII OOH] Rapidly oxidized As(III) to As(V) [72]
Hg Green rusts (mixture of FeII /FeIII hydroxides) Reduced Hg(II) to Hg(0) in suboxic soils and sediments. [73]
Se Green rust In suboxic conditions, green rust reduced Se(VI) to Se(0). [74,75]
Se Zero valent iron Reduced Se(VI) to insoluble selenide (Se(-II)) species. [76]

abiotic and biotic processes [37]. Chromate (Cr(VI)) can be reduced that are subsequently removed by volatilization [86]. Methy-
to Cr(III) in environments where a ready source of electrons (Fe(II)) lated derivatives of As, Hg, and Se can originate from chemical
is available and microbial Cr(VI) reduction occurs in the presence and biological mechanisms and this frequently results in altered
of organic matter as an electron donor [37,81] (Fig. 4). In living sys- volatility, solubility, toxicity, and mobility. Although methyla-
tems, Se tends to be reduced rather than oxidized, and reduction tion of metal(loid)s occurs through both chemical (abiotic) and
occurs under both aerobic and anaerobic conditions. Dissimilatory biological processes, biological methylation (biomethylation) is
Se(IV) reduction to Se(0) by chemical reductants such as sulfide or considered to be the dominant process in soils and aquatic envi-
hydroxylamine, or biochemically by glutathione reductase, is the ronments. Biomethylation may result in metal(loid) detoxification,
major biological transformation for remediation of Se oxyanions since methylated derivatives may be excreted readily from cells,
in anoxic sediments [82]. Hence, precipitation of Se(0), which has and are often volatile and may be less toxic, e.g., organoarsenicals.
been associated with bacterial dissimilatory Se(VI) reduction, has Thayer and Brinckman [87] grouped methylation into two
great environmental significance [83,84]. In the case of Hg, microor- categories: trans-methylation and fission-methylation. Trans-
ganisms, particularly bacteria play a major role in reducing reactive methylation is the transfer of an intact methyl group from one
Hg(II) to non-reactive Hg(0), which may be subjected to volatiliza- compound (methyl donor) to another (methyl acceptor). Fission-
tion losses. Mercury(II) is reduced to Hg(0) by mercuric reductase, methylation is the fission of a compound (methyl source), not
and the dissimilatory reducing bacterium Shewanella oneidensis has necessarily containing a methyl group, so as to eliminate a molecule
been shown to reduce Hg(II) to Hg(0), which requires the presence such as formic acid. The fission molecule is subsequently captured
of electron donors [85]. by another compound which is reduced to a methyl group.
Microorganisms in soils and sediments act as biologically active
3.4. Methylation/demethylation methylators [22,88]. Organic matter provides the methyl-donor
source for both biomethylation and abiotic methylation in soils and
Methylation is a biological mechanism for the removal of toxic sediments. Methylation of Hg is controlled by low molecular weight
metal(loid)s (e.g., Hg) by converting them to methyl derivatives fractions of fulvic acid in soils [89]. Similarly, Lambertsson and Nils-
son [90] suggested that organic matter and alternative electron
acceptors influenced methylation of Hg in the sediments.
600
Biomethylation is effective in forming volatile compounds of
As such as alkylarsines, which could easily be lost to the atmo-
500 sphere [91,92]. Benthic microbes methylate As under both aerobic
Maximum Cr reduction (mg/kg)

and anaerobic conditions to produce methylarsines and methyl-

arsenic compounds with a generic formula (CH3 )n As(O)(OH)3−n .
400
Monomethylarsenate (MMA) and dimethylarsenite (DMA) are
common organoarsenicals in river water. Methylated As species
300 could result from direct excretion by algae or microbes or from
degradation of the excreted arsenicals or more complex cellular
organoarsenicals [93].
200
Methylation of Hg occurs under both aerobic and anaerobic
conditions [94]. Regnell and Tunlid [95] showed that the propor-
100 tion of methylated Hg was significantly higher in the anaerobic
condition than in aerobic systems consisting of undisturbed lake
sediment and water. Under anaerobic conditions Hg(II) ions can be
0
biologically methylated to form either monomethyl or dimethyl Hg
Soil 2+CMB

Soil 3+CMB
Soil 3
Soil 1+BC

Soil 3+BC
Soil 1+CMB

Soil 2
Soil 1

Soil 2+BC

which are highly toxic and more biologically mobile than the other
forms [6]. The main methylation mechanism for Hg involves non-
enzymatic transfer of methyl groups of methylcobalamin to Hg(II)
ions [96].
Fig. 4. Effect of carbon amendments on maximum Cr reduction (mg/kg) in soils
(soil 1, calcic red sandy loam; soil 2, calcic red clay; and soil 3, tannery waste Selenium biomethylation is of interest because it represents
contaminated soil; BC black carbon; CMB chicken manure biochar) [37]. a potential mechanism for removing Se from contaminated
146 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
environments as methylated compounds, such as dimethyl
selenide (DMSe) are less toxic than dissolved Se oxyanions.
Dimethyl selenide can be demethylated in anoxic sediments
as well as anaerobically by an obligate methylotroph similar
to Methanococcides methylutens in pure culture. An anaerobic
demethylation reaction may result in the formation of toxic and
reactive H2 Se from less toxic DMSe. Aerobic demethylation of DMSe
is likely to yield Se(VI), thereby retaining Se in the system.
4. Approaches and indicators of bioavailability
4.1. Approaches to bioavailability
The generic definition of bioavailability is the potential for living
organisms to take up chemicals from food (i.e., oral) or from the
abiotic environment (i.e., external) to the extent that the chemicals
may become involved in the metabolism of the organism. More
specifically, it refers to the biologically available chemical fraction
(or pool) that can be taken up by an organism and can react with
its metabolic machinery [97]; or it refers to the fraction of the total
chemical that can interact with a biological target [98]. In order to
be bioavailable, the contaminants (e.g., metal(loid)s) have to come
in contact with the organism (i.e., physical accessibility). Moreover,
metal(loid)s need to be in a particular form (i.e., chemical accessi-
bility) to be able to enter a plant root. In essence, for a metal(loid)
to be bioavailable, it will have to be mobile and transported across
a membrane and be in an accessible form to the plant.
4.2. Indicators of bioavailability
Bioavailability of metal(loid)s in soils can be examined using
chemical extraction and bioassay tests that determine a fraction of
the metal(loid)s is bioaccessible. Chemical extraction tests include
single extraction and sequential fractionation [99–101]. Bioassay
involves plants, animals, and microorganisms [102,103].
A range of chemical extractants including mineral acids (e.g.,
1 N HCl), salt solutions (e.g., 0.01 M CaCl2 ), buffer solutions (e.g.,
1 M NH4 OAc), and chelating agents [e.g., diethylene triamine pen-
taacetic acid (DTPA)] have been used to predict the bioavailability of
metal(loid)s in soils [104–106]. Chelating agents, such as ethylene-
diamine tetraacetic acid (EDTA – 0.05 M) and 0.05 M DTPA, have
often been found to be more reliable in predicting the plant avail-
ability of metal(loid)s [107,108], since they are more effective in
removing soluble metal(loid)–organic complexes that are poten-
tially bioavailable.
Sequential fractionation schemes are often used to examine the
redistribution or partitioning of metal(loid)s in various chemical
forms that include soluble, adsorbed (exchangeable), precipitated,
organic, and occluded. Although the extraction procedures vary,
generally the solubility and bioavailability of metal(loid)s in soils
decrease with each successive step of the scheme [99,109]. Specific
chemical pools measured by chemical fractionation schemes have
been correlated with plant uptake of metal(loid)s and have been
successful in predicting the plant availability of metal(loid)s in soils
[54,110].
The bioavailability of metal(loid)s in soils has recently been
examined using physiologically based in vitro chemical fraction-
ation schemes that include the Physiologically Based Extraction
Test (PBET), Relative Bioaccessibility Leaching Procedure (RBALP),
Potentially Bioavailable Sequential Extraction (PBASE), and Gas-
trointestinal (GI) Test [111–113]. These innovative tests predict the
bioavailability of metal(loid)s in soil and sediments when ingested
by animals and humans. As in the case of traditional sequen-
tial extraction schemes, the ability of these tests to solubilize
metal(loid)s increases with each successive extraction step. Despite
the recognized nonspecific (i.e., operational) nature of chemical
extraction methods, their analytical simplicity and rapidity ren-
ders them most suitable for routine identification of metal(loid)
form and estimation of the bioavailability of metal(loid)s under
field conditions. However, the distribution of a given metal(loid)
among the various fractions can only be considered as an estimate
at best due to the subjectivity of the steps involved.
Measurements of metal(loid) bioavailability and toxicity in soils
using soil microorganisms are receiving increasing attention, as
microorganisms are more sensitive to heavy-metal(loid) stress
than plants or soil macrofauna [114,115]. The methods using
microflora and protozoa have the potential to provide a mea-
sure of bioavailability of heavy metal(loid)s in the short-term and
even facilitate the measurement of temporal changes. In con-
trast, responses by mesofauna (microarthropods) and macrofauna
(enchytridae, invertebrates, and earthworms) have cumulative
effects. These methods, however, are time consuming and can only
provide an overall effect of heavy metal(loid) bioavailability to the
species tested. Although molecular techniques are rapidly devel-
oped and applied, they are comparatively expensive, and thus the
level of information provided by these techniques need to be clearly
demonstrated [116,117].
5. Soil amendments for remediation
A number of amendments are used either to mobilize or immo-
bilize heavy metal(loid)s in soils. The basic principle involved
in the mobilization technique is to release the metal(loid)s in
to soil solution, which is subsequently removed using higher
plants. In contrast, in the case of the immobilization technique the
metal(loid) concerned is removed from soil solution either through
adsorption, complexation, and precipitation reactions, thereby ren-
dering the metal(loid)s unavailable for human and plant uptake and
leaching to groundwater [12]. In this section the potential value of
these soil amendments in the (im)mobilization of metal(loid)s in
relation to remediation will be discussed.
Kirkham [118] reviewed titles of papers cited in the first 30
issues of Current Contents: Agriculture, Biology and Environmental
Sciences published in 2012 and identified 38 papers dealing with
mobilizing and immobilizing agents. Of the 38 papers, six dealt
with immobilization, 29 dealt with mobilization, and two dealt
with both topics. One paper, by Desaules [119], dealt with meth-
ods evaluating how one can tell if a soil is contaminated naturally or
anthropogenically, and he pointed out that distinguishing between
natural and anthropogenic metal(loid) contents in soils depends
upon values for natural content, which range considerably. The fact
that three-quarters of the papers reviewed by Kirkham [118] con-
sidered mobilization shows that removal of the pollutant is of more
concern than stabilization of the contaminant. This reflects the pos-
sibility that, over time, metal(loid)s once immobilized in the soil
will become available for plant uptake [120–123].
5.1. Mobilization of soil contaminants
Mobilization of contaminants can be achieved through solubi-
lization, desorption, chelation, and complexation reactions which
result in the redistribution of contaminants from solid phase to
solution phase, thereby increasing their bioavailability (Table 2).
5.1.1. Desorbing agents
Addition of P fertilizers to Pb–As(V) contaminated soils has
resulted in an increase in the solubilization and subsequent mobil-
ity of certain oxyanions, such as selenite, As(V), and Cr(VI) in soils
[152–157]. Seaman et al. [158] observed that increasing levels of
hydroxyapatite addition to metal(loid)-contaminated sediments
resulted in increases in the concentrations of Cr(VI) and As(V) in
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166 147

Table 2
Selected references on the potential value of soil amendments in the mobilization of metal(loid)s in soils.

Amendments Metal(loid)s Observations References

Chelating/complexing agents
EDTA (0.1 M, 0.001 M) Cu Mobilized and increased plant uptake. [124]
EDTA, KI, Citric acid Hg Mobilized and increased plant uptake. EDTA showed highest leaching. [125]
EDTA Pb Mobilized and increased plant uptake. [126]
EDTA, EDDS Cu EDTA and EDDS enhanced Cu uptake. EDTA caused a significant growth [127]
reduction. Cu concentrations in soil solution were much higher in EDTA
treatment than EDDS.
EDTA, EDDS Cu Both increased plant uptake, but EDDS was more efficient in [128]
phytoextraction.
EDDS, MGDA Pb, Zn Both Pb and Zn mobilized in soil solution. Plant uptake of Pb was [129]
enhanced, but Zn was unaffected.
EDTA, Citric acid Cd, Cu, Pb, Zn Increased the mobility of all metal(loid)s in soil and enhanced [130]
accumulation of metal(loid)s in aerial parts.
EDTA, EDDS Cu, Pb Plant uptake was only slightly affected by chelate. Cu leaching was higher [131]
than Pb.
EDDS (0.078 M) Cu EDDS significantly increased soluble Cu in the top 5 cm soil layer 1 day [132]
after the application, and the increase of soluble metal(loid) was limited in
the top 20 cm soil. The potential leaching with EDDS may be controlled
under field conditions.
EDTA, EDDS, NTA, Oxalic acid, Citric acid As, Cr, Cu Most effective treatments for stimulating metal(loid) uptake in plant [133]
shoots were EDDS for Cu, EDTA for Cr, and citric acid for As.
Citric acid, EDTA (0.0025 M) Cr, Ni, Ca, Fe, Mg, Al, Mn, Zn Chelants increased leaching of all metal(loid)s showing the dissolution of [134]
soil mineral constituents. EDTA leaches more major elements and Ni than
citric acid due to the respective stability of metal(loid)-chelant complexes;
citric acid leaches more Cr than EDTA, because of a substitution reaction
with Cr(VI).
Citric acid Cd, Pb Citric acid mobilized metal(loid)s, improved the mechanisms of [135]
antioxidative response and phytoextraction in S. nigrum.
Tartaric acid, citric acid Cd, Pb, Zn In comparison to control, citric acid mobilized 71%, 181%, and 112% of Cd, [136]
Pb, and Zn while tartaric acid mobilized 70%, 155%, and 135% of Cd, Pb, and
Zn, respectively.
Humic acid, EDTA Cd Plant uptake enhanced significantly [137]
CCA, EDTA Pb, Zn CCA improved bioavailability in soil, enhanced shoot content of Pb but not [138]
of Zn.
NTA, HEIDA (5–500 ␮M) As, Cu, Zn Application of NTA in As-amended soil and HEIDA in Cu-amended soil at [139]
the rate of 20 mmol/kg increased 3–4-fold of As and Cu in shoot of both
plants (vetiver, maize), whereas application of NTA (20 mmol/kg)
increased 37- and 1.5-fold of Zn accumulation in shoot of vetiver and
maize.
NTA, EDTA, picolinic acid Th(IV) EDTA, NTA and, to a lesser extent, picolinic acid decreased the sorption of [140]
Th to silica, demonstrating the formation and solubility of Th complexes.
However, EDTA and NTA did not sorb significantly to the sand, and
metal(loid) desorption indicated that the mechanism involved exchange
with sand-associated metal(loid)s.
DTPA Se Selenium removal was further increased 12- to 20-fold with 7.5 mmol/kg [141]
EDDS and 1.0 mmol/kg DTPA application, respectively.
Organic matter
Poultry manure Cd, Cu Poultry manure increased the available Cd concentration during three year [142]
study, contrary to Cu.
Rice straw, Clover Cd Increased Cd in Sedum plumbizincicola. No increase in soil solutions. [143]
Biochar, Green waste compost As, Cd, Cu, Zn Copper and As concentrations in soil pore water increased more than 30 [144]
fold after adding both amendments, whereas Zn and Cd decreased
significantly.
Biochar As Biochar increased As in pore water but reduced uptake to tomato plants. [145]
Biochar, sewage sludge Cu, Ni, Pb, Zn Leaching of Cu, Ni and Zn were higher in sewage sludge samples than that [146]
in biochar treatment. Sewage sludge samples reduced plant uptake of Ni,
Zn, Cd and Pb only slightly compared to biochar samples.
Sewage sludge Cu The effect of sewage sludge on Cu in solution and plants depended on the [147]
degree of weathering. In tailings with a low degree of sulfide oxidation,
sludge application resulted in increased solubility and shoot accumulation
of Cu.
Sewage sludge Cd, Pb, Ni Metal(loid) concentrations in mung bean exceeded the permissible limits. [148]
Sewage sludge Cd, Cu, Cr, Ni, Pb, Zn Sewage sludge increased metal(loid) uptake in root and shoot of Beta [149]
vulgaris. Concentrations of Cd, Ni and Zn were more than the permissible
limits.
Sewage sludge, Compost Cd, Cu, Ni, Pb, Zn Amendments increased dry matter, and caused higher concentrations of [150]
metal(loid)s in roots and shoots, but did not exceed the guidelines.
Manure, Sewage sludge, Compost Cd, Cu, Mn, Ni, Pb, Zn Metal(loid)s increased in seeds and grains of spring rape and spring [151]
triticale, but were within the guideline limits.

EDTA, ethylene diaminetetra-acetic acid; KI, potassium iodide; EDDS, ethylene diamine-N,N -disuccinic acid; DTPA, diethylenetriamine pentaacetate; MGDA, methyl glycine
diacetic acid; NTA, nitrilotriacetic acid; HEIDA, hydroxyethylimino diacetic acid; CCA, coated chelating agent.
148 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Fig. 5. Phosphate (H2 PO4 − ) ions compete for As(V) adsorption by soil particles (a),
and for As(V) absorption by plant roots (b) [170].
solution. This is attributed to increased adsorption competition
by H2 PO4 − ions with the oxyanions [156,159–161]. However, the
effect of H2 PO4 − on metal(loid) desorption depends on the nature
of the soil, its sorption capacity, and the extent of saturation with
a particular metal(loid) ion [162].
Phosphate has also been shown to strongly compete with the
molybdate anion (MoO4 2− ) for adsorption sites, thereby resulting
in increased desorption of the latter [159,163,164]. Nuenhauserer
et al. [165] demonstrated the value of P fertilizers in the phytore-
mediation of Mo-contaminated soils, where application of soluble
P fertilizer greatly enhanced the solubilization of Mo in a soil con-
taminated with excess Mo, facilitating its removal through plant
uptake.
Phosphorus influences As uptake by plants by two processes.
Firstly, it is well known that As(V) acts as a P analog and is taken
up by plants via a P transporter system [166]. While P deficiency
can enhance As uptake, high concentration of P in soil solution can
inhibit the uptake of As [167,168]. Secondly, P is more strongly
adsorbed to soil than As(V) and hence competes for sorption sites,
thereby facilitating the desorption of As to soil solution and its
subsequent uptake by plants [169]. Thus the influence of P on As
mobilization depends on the charge characteristics of soils.
Bolan et al. [170] reported that the effect of P on the mobi-
lization and bioavailability of As varied between allophanic and
non-allophanic soils and also between soil system and solution cul-
ture. The P-induced impact on plant uptake of As in solution culture
and soil system can be attributed to competition of P for both As
adsorption by soil particles and absorption by plant roots (Fig. 5). In
the solution culture system, P addition competed for As absorption
by plant roots thereby decreasing its uptake. In the soil system, P
addition facilitated the desorption and bioavailability of As. How-
ever, the net effect of P on As phytoavailability in soils depends
on the extent of P-induced As mobilization in soils and P-induced
competition for As uptake by roots (Fig. 5).
5.1.2. Chelating agents
Chelating agents which have high affinity for metal(loid)
ions can be used to enhance the solubilization of metal(loid)s
in soils through the formation of soluble metal(loid) chelates
(Fig. 6). A number of synthetic chelating agents are avail-
able including amino polycarboxylates, such as EDTA, DTPA,
ethylenediamine-N,N -bis(2-hydroxyphenylacetic acid) (EDDHA),
N,N -ethylenebis-[2-(o-hydroxyphenyl)]-glycine (EHPG) and many
others (Table 2).
400 Cu
Pb
300
Metals extracted (mg/kg)
200
100
40
30
20
10
0
1 2 3 4 5 6 1 2 3 4 5 6
Silty Loam San d
Fig. 6. Total amounts of Cu and Pb extracted from soils by various chelating agents;
(1) EDTA, (2) EDDS, (3) histidine, (4) glycine, (5) citric acid, (6) tartaric acid [131].
The value of chelating agents in enhancing the availability of
heavy metal(loid)s such as Fe, Cu, and Zn has been well rec-
ognized in plant nutrition and various chelated compounds are
available as nutrient sources. The potential value of chelating
agents in the remediation of contaminated soils through mobiliza-
tion of metal(loid)s has been explored [124,171]. These compounds
have been found to be very effective in the mobilization of
metal(loid)s such as Cu and Pb, thereby enhancing their subsequent
uptake by plants. The effectiveness of any chelate in mobilizing
soil metal(loid)s depends on several factors, including metal(loid)
species, metal(loid):chelate ratio, thermodynamic stability con-
stants, presence of competing cations, soil pH, stability of the
metal(loid)–chelate complex, extent of metal(loid) retention onto
soil constituents, and the aging of the contaminating metal(loid).
Recently there has been interest in the use of complexing agents
such as thiosulphate in mobilizing Hg in soils. For example, Moreno
et al. [172] demonstrated that the addition of sulphur containing
ligand compounds such as sodium or ammonium thiosulphate to
mine tailings contaminated with Hg can induce the solubilization
of Hg and its subsequent uptake and accumulation in both roots
and shoots of plants. They noticed that the concentration of Hg
in Brassica juncea plants reached a maximum of 85 mg/kg when
the plants were grown in a soil with an Hg content of 3.4 mg/kg,
thereby reaching a maximum transfer factor (i.e., the ratio between
plant and soil concentration) of 25. Moreno et al. [173] described a
field demonstration for Hg phytoremediation conducted at a base-
metal(loid) tailings site in the Coromandel district of New Zealand.
These authors showed that Hg uptake could be induced in the field,
although the results were generally variable.
Mercury is a metal(loid) often targeted for remediation
through volatilization. Transgenic plants encoding genes from Hg-
detoxifying bacteria that have increased resistance and enhanced
volatilization capacity are able to extract Hg(II) and methyl mer-
cury from contaminated soil and convert these forms to Hg(0). This
less toxic form of the metal(loid) is then released as Hg vapour into
the atmosphere [174–176]. Moreno et al. [173] observed that appli-
cation of thiosulphate to soil reduced the amount of Hg volatilized
by B. juncea plants, as well as increasing the Hg concentration
stored in the plant tissues. During an experiment conducted in
sealed volatilization chambers, the daily amount of Hg volatilized
from planted mine tailings irrigated with water was recorded
as 23 times greater than the amount released from non-planted
mine tailings, but the daily amount of Hg volatilized from planted
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
tailings irrigated with thiosulphate solution was only 6 times
greater than the amount released from the non-planted control.
There is a potential to increase the uptake of a wide range of
metal(loid)s into plants through the judicious application of chem-
icals to soil. But as discussed above for Hg the effect of this increased
uptake on other physiological functions, such as volatilization, must
also be considered. Kirkham [177] suggested using the chelating
agent, EDTA, to increase uptake of metal(loid)s by plants grown
with sewage sludge (also called biosolids). The results showed
that EDTA increased metal(loid) uptake by sunflower (Helianthus
annuus L.). Subsequent work done in a greenhouse [178,179] or at
a sludge farm [180,181] confirmed these results for sunflower and
hybrid poplar (Populus deltoides Marsh. × P. nigra L.). To increase
root growth, Liphadzi et al. [182] noted that addition of auxin
increased root growth and uptake of Mn and Ni, but only when no
EDTA was present. Root growth was decreased in the presence of
EDTA. Nevertheless, the results showed that auxins might be used
to increase root growth for phytoremediation.
5.1.3. Organic amendments
Addition of organic amendments, such as sewage sludge and
green waste composts to soils enhances the physicochemical and
biological conditions of soils, thereby improving plant growth.
Some of these amendments are known to have immobilizing effects
on metal(loid)s because humic acids present bind metal(loid)s such
as Cd, Pb, Cu, and Cr [183–186]. However, the organic amendments
can directly or indirectly alter the distribution and availability of
metal(loid)s in soil [186,187].
The effect of organic residues in the mobility and bioavailabil-
ity of metal(loid)s in soils depends on the specific metal(loid), soil
type, and the characteristics of the amendment (EC, CEC, pH, and
humification degree) [186–189]. For instance, there are reports
that amending contaminated soils with compost may increase
the mobility and leaching of metal(loid)s [190], particularly As
[191–193]. Large increases in leachable As from soils amended with
compost were observed, probably due to DOC competing with As
for sorption sites such as those on iron-oxide surfaces, causing
increased As mobility and subsequent plant uptake [194]. Com-
posts may also possess a significant soluble P component which
can displace As from organic and inorganic binding sites while ful-
vic acids can have a similar effect [195–198]. In contrast, Cao and
Ma [199] used compost to remediate CCA contaminated soils and
reported a positive effect on As adsorption, as found by others after
compost application [200,201]. In another study, the concentration
of As in the above-ground growth of pearl millet was highest in the
compost-amended soils and the foliage contained toxic levels of As,
but the millet seed head As concentrations were below toxic lev-
els [202]. Moreno-Jiménez et al. [203] observed the mobilization
of As, Cu, and Se in flooded soils after the application of olive mill
waste compost which they attributed to increased pore water DOC
concentrations. They also suggested that, P added in the compost
could partly be responsible for the mobilization of As.
Fleming et al. [204] estimated Pb and As availability by earth-
worm bioassay in the presence of compost and noticed a reduction
of Pb bioavailability but not As. Udovic and McBride [205] assessed
the remediation efficiency of compost addition, in decreasing the
human exposure to Pb and As by direct ingestion. A number of
bioavailability tests showed that compost addition consistently
decreased Pb, but increased As potential bioavailability.
Biochars have been shown to reduce the mobility of some
organic and inorganic pollutants in soil. Source material and pro-
duction conditions of biochars can influence pollutant retention.
Highly alkaline pH and water soluble carbon can undesirably mobi-
lize some elements. Beesley et al. [145] observed that, while the
solubility and mobility of As were increased by biochar addition
to soil, uptake to plant was reduced, and toxicity-transfer risk
149
was negligible. Clemente et al. [190] investigated the mobility of
metal(loids)s including As and Sb, two years after the application
of compost mulch. Compost mulch increased organic carbon and
Fe in soil pore water, which in turn increased As and Sb mobiliza-
tion; this enhanced uptake by lettuce and sunflower. Sorption of
Cd and Zn to biochar’s surfaces assisted a 300 and 45-fold reduc-
tion in their leachate concentrations, respectively, but the leachate
concentrations of As did not duly decline [206].
Wu et al. [143] reported that traditional organic materi-
als (rice straw and clover) can be much more effective and
environmentally friendly amendments than the chelating agent,
Ethylenediamine-N,N -disuccinic acid (EDDS) in enhancing phy-
toremediation efficiency of Cd contaminated soil. Wang et al.
[207] reported that, arbuscular mycorrhizal fungi and organic
manure play a synergistic positive role both in phytoextraction
and phytostabilization of Cd and Pb. However, in some other occa-
sions, these amendments can also add soluble organic ligands,
thereby increasing metal(loid) mobility and leaching to ground-
water [208,209]. The amount of organic matter has been shown to
affect metal(loid) movement in soil.
5.1.4. Fertilizers
In addition to chelating agents, inorganic fertilizers have been
shown to be mobilizing agents. Kirkham [118] identified two
papers that studied mobilization of heavy metal(loid)s using
fertilizers [210,211]. Munksgaard et al. [210] showed that super-
phosphate fertilizer had opposing effects on metal and metalloid
mobility when applied to soils contaminated with mine wastes. The
contaminated soils contained sulfide and sulfate-rich waste mate-
rial from mining sites in Australia. Results of long-term (10 months)
column experiments showed that the fertilizer was ineffective in
stabilizing highly soluble metal-bearing phases in a sulfate-rich
soil. In a sulfide-rich soil with abundant organic matter, complex-
ing of metal(loid)s with soluble organic acids led to pronounced
metal(loid) (mainly Cd, Cu, and Zn) release from fertilizer-amended
soils. The abundance of pyrite, as well as the addition of fertilizer,
caused persistent acid production over time, which prevented the
formation of insoluble metal(loid) P phases and instead fostered
an increased mobility of both metals and metalloids [210]. By con-
trast, fertilizer application to a sulfide-rich soil with low organic
carbon content and a sufficient acid buffering capacity to maintain
near-neutral pH resulted in the immobilization of Pb in the form of
newly precipitated Pb–P phases.
Tanhan et al. [211] conducted greenhouse and field experi-
ments to evaluate the use of Chromolaena odorata (L). King &
Robinson, a perennial shrub in Thailand, for phytoextraction of
Pb contaminated soil that was treated with EDTA. Control soils
received no EDTA. Lead-mine soils are low in fertility, so they
added organic (cow manure) and inorganic (Osmocote, NH4 NO3 ,
and KCl) fertilizers to enhance plant growth and Pb accumulation.
The greenhouse study showed that cow manure decreased avail-
able Pb concentrations, but, nevertheless, this treatment resulted
in the highest Pb concentrations in roots and shoots. The chelate
EDTA increased Pb accumulation in roots and shoots in soil with
Osmocote. Tanhan et al. [211] concluded that Pb accumulation
could be enhanced by Osmocote fertilizer. However, they warned
that the use of EDTA in the field is of concern due to leach-
ing of the toxic heavy metal(loid), Pb. Three other papers in the
review of Kirkham [98] also pointed out increased leaching of
heavy metal(loid)s with EDTA [134,212,213], which may lead to
groundwater contamination. Madrid et al. [214] and Liphadzi and
Kirkham [179,215] also noted that EDTA leaches heavy metal(loid)s
out of the soil, and Madrid et al. [214] suggested that EDTA still
could be used in phytoremediation if the drainage water were con-
tained.
150 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
5.1.5. Saline waters
Because no information existed concerning the consequences
of saline-water irrigation on the mobility of heavy metal(loid)s
in sludge applied to soil during phytoremediation, Wahla and
Kirkham [216] determined the effect of NaCl irrigation on the dis-
placement of seven metal(loid)s (Cd, Cu, Fe, Mn, Ni, Pb, and Zn)
in sludge applied to the surface of soil columns containing bar-
ley (Hordeum vulgare L.) plants. Half of the columns were treated
with EDTA. With EDTA, concentrations of the metal(loid)s in the
drainage water were higher with NaCl irrigation than with tap-
water irrigation. Even with no EDTA, irrigation with the NaCl
solution increased the concentration of Cd, Fe, Mn, and Pb in
the drainage water above drinking-water standards. Wahla and
Kirkham [216] concluded that irrigation of sludge farms with brack-
ish water is not recommended, because saline water increased the
mobility of the metal(loid)s and they polluted the drainage water.
5.1.6. Microbial mobilization
Microorganisms play a vital role in the transformation of trace
elements thereby influencing their bioavailability and remediation.
They may alter the toxicity, water solubility and/or mobility of the
element [217]. The increase in the solubility and mobility can be uti-
lized to bioremediate insoluble forms of elements in soil because
the biotransformed product is released from the solid phase into
the solution phase. Also, a decrease in the solubility of elements
can be used to remove it from surface or groundwater through
immobilization. Sometimes, the gaseous metal(loid) products can
be removed through volatilization [218].
Genetically engineered microorganisms (e.g., Escherichia coli)
which express metal(loid) binding protein (i.e., metallothionein)
and a metal(loid)-specific transport system have been found
to be successful in their selectivity for accumulation of a spe-
cific metal(loid) in the presence of high concentration of other
metal(loid)s and chelating agents in solution [219,220]. These
organisms have the potential to remove specific metal(loid)s from
contaminated soil and sediments by washing them with chelating
agents and then regenerating the chelating agents by passing the
solution through reactor containing the microbial strain [221,222].
Dissimilatory reduction of As, Se, and possibly other metal(loid)s
can convert soluble metal(loid) species to insoluble forms that can
readily be removed from contaminated waters or waste streams
[223]. Reduction of Hg can volatilize Hg from surface water and
ocean [172,173,224]. Arsenic can be reduced to As(0), which is
subsequently precipitated as As2 S3 as a result of microbial sul-
fate reduction. Because As(III) is more soluble than As(V), the latter
can be reduced using bacteria in soil and subsequently leached.
Conversely, As(III) is oxidized to As(V) using microbes which is
subsequently precipitated using ferric ions [225,226]. Bahar et al.
[227] isolated a new As(III)-oxidizing bacterium Stenotrophomonas
sp. from a low As-containing soil. Batch experiment results showed
that the strain completely oxidized 500 ␮M of As(III) to As(V) within
12 h of incubation in a minimal salts medium at an optimum pH
range of 5–7. Desulfototomaculum auripigmentum, which reduces
both As(V) to As(III) and sulfate to H2 S, leads to As2 S3 precipitation
[228]. Chemolithotropic bacteria play a major role in the oxidation
process, thereby enhancing the mobilization of metal(loid)s. The
use of fungi species offers a way to leach As from industrial waste
sites [229]. The production of organic acids with the use of het-
erotrophic organisms, and the generation of sulphuric acid with the
use of microorganisms, such as Thiobacillus, offers some promising
approach to the extraction of As [230].
Bender et al. [231] substantiated the commercial application of
microbial mats developed by combining cyanobacteria inoculum
with a sediment inoculum from a metal(loid)-contaminated site for
the removal and transformation of metal(loid)s. The mat tolerated
high concentrations of toxic metal(loid)s, such as Cd, Pb, Cr, Se, and
As (up to 350 mg/L) and achieved a rapid removal of the metal(loid)s
from contaminated water. The mats produced metal(loid)-binding
polyanionic polysaccharides, deposited the metal(loid) compounds
outside the cell surfaces, and chemically modified the aqueous
environment surrounding the mat, thereby managing the toxic
metal(loid)s. Thus, depending on the chemical characteristics of the
mat, the sequestered metal(loid)s could be oxidized, reduced, and
precipitated as sulfides or oxides. Precipitates of red amorphous
Se(0), for instance, were identified in the mat exposed to Se(VI).
5.2. Immobilization (stabilization) of soil contaminants
Immobilization of contaminants can be achieved mainly
through adsorption, precipitation, and complexation reactions
which result in the redistribution of contaminants from solution
phase to solid phase, thereby reducing their bioavailability and
transport in the environment [71].
5.2.1. Phosphate compounds
A large number of studies have provided conclusive evidence
for the mitigative value of both water-soluble (e.g., diammonium
phosphate, DAP) and water-insoluble (e.g., apatite, also known as
PR) P compounds to immobilize metal(loid)s in soils, thereby reduc-
ing their bioavailability for human and plant uptake and mobility
for transport [12,46] (Table 3). Phosphate compounds enhance
the immobilization of metal(loid)s in soils through various pro-
cesses including direct metal(loid) adsorption/substitution by P
compounds, P anion-induced metal(loid) adsorption, and precip-
itation of metal(loid)s with solution P as metal(loid) phosphates.
Depending on the source, soil application of P compounds can cause
direct adsorption of metal(loid)s onto these compounds through
increased surface charge and enhanced anion-induced metal(loid)
adsorption.
Precipitation as metal(loid)–P has been proved one of the main
mechanisms for the immobilization of metals, such as Pb and Zn,
in soils. These fairly stable metal–P compounds have extremely
low solubility over a wide pH range, which makes P application
an attractive technology for managing metal(loid)-contaminated
soils. In typical arable soils, precipitation of metal(loid)s is unlikely,
but in modest metal(loid)-contaminated soils, this process can play
a major role in the immobilization of such metal(loid)s.
The ability of apatite to immobilize Pb in solution or Pb
in contaminated soils through precipitation as Pb–P has been
well documented (e.g., Chrysochoou et al. [273]). Such precip-
itates are more commonly manifested as hydroxypyromorphite
or as chloropyromorphite [274]. Two processes for the reaction
of dissolved Pb with apatite have been proposed. Firstly, Pb(II)
can substitute for Ca(II) in apatite. Thus (Ca, Pb) apatite could
be potentially formed by adsorption of Pb or by dissolution of
hydroxyapatite (Ca10 (PO4 )6 (OH)2 ) followed by coprecipitation of
mixed apatites. Secondly, Pb2+ can react with apatite through
hydroxyapatite dissolution, followed by precipitation of pure
hydroxypyromorphite (Pb10 (PO4 )6 (OH)2 ). The addition of P in
Zn contaminated sediments resulted in precipitation of hopeite
[275,276]. Coprecipitation of radioactive strontium with Ca–, Al–,
and Fe–P compounds in contaminated soils was reported as a useful
in situ immobilization technology for Sr-contaminated sites [277].
Soils which have a high affinity for ligand anions may enhance
metal(loid) ion adsorption through modifications in the soil sur-
face charge density. It has often been shown that the adsorption
of specifically sorbing ligands such as HPO4 2− in strongly weath-
ered and variable charge soils can induce Cd(II) adsorption through
increased negative surface charge [41,51]. An alternate mecha-
nism, which appears to be important in temperate soils, involves
metal–ligand complexation in solution and subsequent reduction
in cation charge, which probably reduces adsorption [47]. The
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166 151

Table 3
Selected references on the potential value of soil amendments in the immobilization of metal(loid)s in soils.

Amendments Metal(loid)s Observations References

Phosphate compounds
KH2 PO4 Cd Enhanced immobilization, decreased plant availability. [46]
Apatate, zeolite, Fe-oxide Cd, Pb Reduced the mobility and uptake by plant. [232]
KH2 PO2 Pb, Zn, Cd Reduced Pb level but not Zn and Cd in earthworms. [233]
Phosphate As Increasing phosphate supply decreased As uptake. Increasing As [234]
supply decreased the P concentration in the root.
Phosphate Pb, As Increased plant uptake of soil As. No effect on soil Pb [235]
phytoavailability.
H3 PO4 , Ca(H2 PO4 ), phosphate rock Pb, Zn, Cu Increased residual fraction of Pb, Zn and Cu, and reduced metal [236]
(loid) translocation from root to shoot of plant.
Phosphate rock, diammonium phopshate Cd, Pb, Zn Reduced metal(loid) elution. [237]
Bonemeal (finely ground, poorly crystalline Pb, Zn Reduced metal(loid) concentration in the leachate and availability [238]
apatite) of metal(loid)s in soils.
Hydroxyapatite, phosphate rock, triple Cd, Pb, Zn Reduced metal(loid) uptake by plant. [239]
superphosphate, diammonium phosphate
Vivianite Cu Reduced leachability and in vitro bioaccessibility of Cu in soils. [240]
Liming materials
Ca(OH)2 Cd Transformed to less mobile fractions, reduced phytoavailability. [241]
Lime, FBA, Bark Cr Reduced the availability for plant uptake and leaching ground [62]
water.
Lime Cd Did not reduce uptake and transfer to the kernels of sunflower. [242]
Lime Cd Reduced uptake by lettuce. [243]
Lime Pb, Cd Decreased Cd uptake, but little influence Pb uptake by radish. [244]
Ca(OH)2 , CaCO3 Cd Ca(OH)2 prevented phytotoxcicity, but CaCO3 was no effective in [245]
reducing phytotoxicity.
Lime Cd, Ni, Zn, Cu Reduced uptake of Cd, Ni, Zn, but did not reduce Cu. [246]
Red mud, natural zeolite, lime Pb, Cd, Zn Reduced solubility of Pb, Cd and Zn, Changes in microbial [247]
communities.
Zeolite, compost, calcium hydroxide Pb, Cd, Zn Increased residual fraction of metal(loid)s in soils and decreased [248]
metal(loid) uptake by white lupin.
Lime, red mud Zn, Cd, Pb, Ni, Cu Reduced grass metal(loid) concentrations. [249]
Cyclonic ashes, lime Zn, Cd Reduced metal(loid) accumulation in plant and Zn and Cd [250]
concentrations in soil pore water.
Lime As Increased As immobilization by the formation of Ca–As [251]
precipitates.
Organic matter
Biosolid Cd Reduced the bioavailability. [252]
Biosolid, manure Cu Reduced the phytotoxic effect. [253]
PS, SS Cd, Zn Cd uptake increased, but Zn unaffected. [254]
Biosolid Cd Reduced plant availability. [255]
Biosolid Zn Decreased plant availability. [256]
Biosolid Cd Cl-complexation of Cd increased the phytoavailability of Cd in [257]
biosolid amended soil.
Organic matter Ni, Cd, Zn Reduced Ni uptake but not Cd, Zn in rice. [258]
Compost, manure Cr Reduced the phytotoxicity. [259]
Chicken manure compost Cd Reduced soluble/exchangeable Cd and phytotoxicity of Cd. [260]
Compost Cd, Cu, Pb, Zn Zn and Cd leaching decreased, but Cu and Pb leaching increased. [261]
Coal fly ash, peat Cu, Pb Reduced metal(loid) leaching in the field lysimeters. [262]
Humus, compost Cd Reduced Cd uptake by rice. [263]
Biosolid, wood ash, K2 SO4 Pb, Zn, Cd Alleviated phytotoxicity of Pb, Zn and Cd and reduced [264]
bioavailability of Pb.
Hard wood biochar Cd, Zn Biochar immobilized metal(loid)s due to enhanced pH. [144]
Chicken manure and green waste biochars Cd, Cu, Pb Immobilization due to partitioning of metal(loid)s from the [265]
exchangeable phase to organic-bound fraction.
Oak-wood biochar Pb Sorbed Pb by increasing the soil pH. [266]
Chicken manure biochar Cr Enhanced soil Cr(VI) reduction to Cr(III). [37]
Metal oxides
Hydrous Mn oxide Cd, Zn, Pb Reduced mobility of Cd, Zn and Pb and uptake of metal(loid)s by [267]
ryegrass.
Mn oxide Pb Reduced bioavailable Pb. [268]
Fe-rich waste (Fe (hydr)oxides) with redox Cd, Cu, Ni, Pb, Zn Reduced exchangeable Cd, Cu, Zn and Pb. [269]
cycles
Mn oxide Cd, Pb Reduced exchangeable fraction of Cd and Pb, and uptake of [270]
metal(loid)s by Chinese cabbage.
Goethite, iron grit, iron (II) and (III) sulphate As, Cu, Zn Reduced plant shoot As content [271]
Fe oxide waste by-product Cd, Pb Reduced uptake of Cd and Pb by maize and barley [272]

FBA, fluidised bed boiler ash; PS, papermill sludge; SS, sewage sludge.

decrease in Cd(II) sorption on to soils in the presence of P [278] was
attributed to the formation of soluble Cd–P complexes. This is con-
sistent with the concept that free Cd(II) activity, rather than total
dissolved Cd(II) concentration, is a controlling factor in Cd(II) sorp-
tion [279].The efficiency of P-induced metal(loid) immobilization
in soil can be enhanced by increasing solubility of P compounds.
Co-application of phosphoric acid and rock phosphate effectively
immobilized Pb and Zn [191]. Phosphate solubilizing bacteria were
employed to increase Pb immobilization in soil by slowly releasing
P from insoluble P rock [280,281] (Fig. 7). There are several concerns
in regarding the application of P compounds for metal(loid) immo-
bilization. The leaching of P induced after P treatment should be
152 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166

25 of Ni. In these cases, the effect of liming materials in decreasing

metal(loid) uptake by plants has been attributed to both decreased
Without PSB
With PSB mobility in soils (through adsorption/precipitation) and to the com-
NH 4NO3 extractable Pb (mg/kg)

20 petition between Ca(II) and metal(loid)s ions on the root surface.

15
10
5
0
S STP
Amendments
Fig. 7. Immobilization of Pb by phosphate amendments and phosphate solubilizing
bacteria (PSB) (S: soil, STP: soil + tricalcium phosphate, SHA: soil + hydroxyapatite,
SPR: soil + rock phosphate) [280].
considered. Zupančič et al. [157] showed that a mixture of soil with
P addition in the molar ratio of H3 PO4 :hydroxyapatite of 0.75:1 was
the optimum to minimize phosphorus leaching.
5.2.2. Liming materials
Although liming is primarily aimed at ameliorating soil acidity,
it is increasingly being accepted as an important management tool
in reducing the toxicity of heavy metal(loid)s in soils (Fig. 8). A
range of liming materials is available, which vary in their ability to
neutralize the acidity (Table 3).
Liming, as part of the normal cultural practices, has often
been shown to reduce the concentration of Cd, Pb, and other
metal(loid)s in edible parts of crops. Liming enhances sorption of
heavy metal(loid)s by reducing the H+ concentration and increas-
ing negatively charged sites. The addition of alkaline materials such
as red mud and lime in a contaminated soil increased the con-
centration of the residual fraction of Pb and Cd. The pH increase
induced by red mud and lime resulted in the precipitation of
heavy metal(loid)s [247]. Similarly liming serpentine soils contain-
ing toxic levels of Ni has shown to alleviate the phytotoxic effects
8.0
7.0
Concentration (mg/kg)
A field trial of in situ remediation of a heavy metal(loid) contami-
nated soil showed that lime and red mud addition increased soil pH
and decreased metal(loid) availability, thereby establishing vege-
tative cover in contaminated soil with a range of heavy metal(loid)s
including Pb, Zn, Cd, and Cu [249].
Lime can be used as a co-amendment to reduce the availabil-
ity of heavy metal(loid)s in soil amendments. Lime increased pH
and decreased electrical conductivity (EC) through precipitation
of soluble ions when it was mixed with biosolids. Water-soluble
and DTPA-extractable Cu, Mn, Zn, and Ni were reduced in
lime-amended biosolids [284]. Lime treatment in composting sig-
nificantly reduced the bioavailability and leachability of heavy
SHA SPR
metal(loid)s by effectively increasing pH [285].
Removal of Cr(III) from industrial effluent is achieved using lime
or magnesium oxide to precipitate as chromic hydroxide. Precip-
itation is reported to be most effective at pH 8.5–9.5 due to the
low solubility of chromic hydroxide in that range. This method
can decrease Cr concentrations to very low levels and hence pre-
cipitation systems are very widely accepted by major tanneries.
Nevertheless, caution should be taken when using lime in Cr con-
taminated soil. Increased soil pH above neutral favors the oxidation
of Cr(III) to the more mobile and toxic Cr(VI) [286,287], which can
negatively affect vegetation [288] and ecosystem health.
5.2.3. Organic composts
The major sources of organic composts include biosolids and
animal manures. Traditionally biosolids are viewed as one of major
sources of metal(loid) accumulation in soils. Advances in the treat-
ment of sewage water and isolation of industrial wastewater in
the sewage treatment plants have resulted in a steady decline
in the metal(loid) content of biosolids. Furthermore, stabiliza-
tion using alkaline materials has resulted in the immobilization
of metal(loid)s in biosolids. Zeolites are also useful as metal(loid)
scavengers in biosolids containing metal(loid)s. The natural zeo-
lite immobilized Cd, Cu, Cr, Fe, Mn, Ni, Pb, and Zn in biosolids,
which transformed metal(loid)s in the exchangeable and carbonate
fractions to residual fractions [289].
Confined animal agriculture (i.e., beef cattle, dairy, poultry, and
swine) is the major source of manure byproducts in most countries.
Most manure products contain low levels of heavy metal(loid)s
Cd
(except Cu and Zn in swine manure and As in poultry manure).
Pb
Furthermore, recent advances in the treatment of manure byprod-
ucts have resulted in reduced bioavailability of metal(loid)s. For

6.0 example, 87% reduction in Cu and Zn in the wastewater from swine

houses was obtained after treatment with lime slurry, ferric chlo-
ride, or polymer. Similarly treatment of poultry manure with alum
5.0
1.5
[Al2 (SO4 )3 ] decreased the concentration of water-soluble As, Zn, Cu,
and Cd. Hence unlike biosolids application, where land application
is limited based on allowable trace element loadings, regulations
1.0
governing livestock and poultry manure byproducts are generally
based on total N and P loading. Manure byproducts that are low in
0.5 metal(loid) content can be used to immobilize metal(loid)s in soils.
Although a number of studies have examined the role of
biosolids as a source of metal(loid) contamination in soil, only
0.0
d te te ell ell ell ell limited work has been reported on the beneficial effect of organic
ate na na sh sh sh sh
tre rbo rbo gg gg ter ter amendments as a sink for the immobilization of metal(loid)s in
Un c a c a e e
oy s
oy s
m m 1% 5%
lciu lciu 1% 5% soils [290,291]. Recent studies have shown that alkaline-stabilized
ca ca
1% 5%
biosolids that are low in total and/or bioavailable metal(loid) con-
tent (known as ‘exceptional quality’ biosolids or ‘designer sludge’)
Fig. 8. Immobilization of Cd and Pb by calcium carbonate, eggshell, and oyster shell
as measured by Cd and Pb concentrations in soil extracted with 1 M calcium chloride can be used as an effective sink for reducing the bioavailability
after treatments [282,283]. of metal(loid)s in contaminated soils and sediments (Table 3).
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Immobilization of metal(loid)s by such amendments is achieved
through adsorption, complexation, and redox reactions.
Addition of organic amendments has often been shown to
increase the cation exchange capacity of soils, thereby resulting
in increased metal(loid) adsorption. The presence of P, aluminum
(Al) compounds, and other inorganic minerals in some organic
amendments, such as typical municipal biosolids, is also believed
to be responsible for the retention of metals, thereby inducing
the ‘plateau effect’ in metal(loid) uptake by crops and preventing
the increased metal(loid) availability suggested in the ‘time bomb’
hypothesis.
Metal(loid)s form both soluble and insoluble complexes with
organic constituents in soils, and the processes apparently depend
on the nature of the organic matter. As might be expected, the
organic component of soil constituents has a high affinity for
metal(loid) cations because of the presence of ligands or functional
groups that can form chelates with metals. With increasing pH,
the carboxyl, phenolic, alcoholic, and carbonyl functional groups in
soil organic matter dissociate, thereby increasing the affinity of lig-
and ions for metal(loid) cations. Manure application significantly
increased shoot growth of Chenopodium album L. and decreased
shoot Cu, Zn, and Mn concentrations in contaminated soil with
pyritic waste from mine spill. The reduction of metal(loid) concen-
trations can be attributed to an increase of soil pH by preventing
sulfide oxidation/hydrolysis [186]. Similarly, compost amendment
enhanced the growth of white lupin (Lupinus albus) and reduced
uptake of Pb and Zn by decreasing bioavailability of metal(loid)s in
the soils [248]. The high metal(loid) binding capacities of compost
was attributed to high compost humic and fulvic acid concentra-
tions [184,292].
A number of studies have shown that addition of organic soil
amendments enhances the reduction of metal(loids) such as Cr
and Se. For example, the addition of cattle manure has resulted
in the reduction of Cr(VI) to less toxic and less mobile Cr(III) [259].
Although Cr(VI) reduction can occur through both chemical and
biological processes, the biological reduction is considered to be
the dominant process in most agricultural soils which are low in
ferrous [Fe(II)] ions, and the addition of manure compost is likely
to increase the biological reduction of Cr(VI).
5.2.4. Metal oxides
Oxides of metals, such as Fe, Al, and Mn, play an important role in
metal(loid) geochemistry in soils. Large, active surface areas and the
amphoteric nature of oxides make them suitable for sorption and
immobilization of a wide range of soil contaminants (Table 3). Metal
oxides can strongly bind metal(loid)s through specific sorption, co-
precipitation, and by forming inner-sphere complexes. Naturally
occurring oxides, synthesized oxide particles, as well as industrial
by-products, have been studied for their suitability to be used for
soil remediation purposes [293]. Latest research efforts of using
metal oxides and their precursors for chemical immobilization of
metal(loid)s in contaminated soils are reviewed by Komárek et al.
[294].
Iron oxides (hematite, maghemite, and magnetite), oxyhy-
droxides (ferrihydrite, goethite, akaganeite, lepidocrocite, and
feroxyhite), and Mn oxides (phyllomanganates and birnessite
group of minerals) are common in soils. Zinc, Cd, and Pb form
mononuclear complexes on goethite and ferrihydrite surfaces,
and AsO4 3− and Pb(II) form inner sphere surface complexes with
hydrous ferric oxide [295]. Surfaces of iron hydrous oxides play
an important role in the retention of As anions. Positive sur-
face charge leads to adsorption of As anions, and adsorption of
As increases at low pH because the surfaces of many oxides are
positively charged. Goethite, iron grit, and Fe(II) and Fe(II) sul-
fates significantly reduced As concentrations in leachates from As
contaminated soils through a series of leachate extraction tests.
153
However, other trace metal(loid)s such as Cd and Pb were mobilized
with incorporation of iron (II) and (III) sulfates [296]. The benefi-
cial re-use of iron oxide-based drinking water treatment residuals
demonstrates very effective retention of As and may be a suitable
soil amendment for a number of anions and cations [297].
Manganese oxide minerals occur in soils, which include bir-
nessite, todorokite, cryptomelane, and hausmannite. Among these
Mn oxide minerals, birnessite showed the greatest adsorption
capacity on Pb, Cu, Co, Cd, and Zn. The order of maxi-
mum sorption capacity of heavy metal(loid)s by birnessite was
Pb(II) > Cu(II) > Zn(II) > Co(II) > Cd(II). The maximum adsorption of
metal(loid)s by birnessite was related to the hydrolysis constants,
which indicates that metal(loid) adsorption by Mn oxide occurs
mainly in the form of hydroxylation cations [298]. Manganese (IV)
oxides are known to specifically adsorb Pb. Hettiarachchi et al.
[268] showed that cryptomelane which was used as the representa-
tive Mn oxide reduced bioavailable Pb. Manganese oxide minerals
oxidized Cr(III) to Cr(VI) and Mn(II) was released during Cr(III)
oxidation. However, released Mn(II) was re-adsorbed on the nega-
tively charged surfaces of the Mn minerals. The oxidation of Cr(III)
occurs by adsorption of Cr(III) on the surface of Mn minerals and
subsequent oxidation of Cr(III) to Cr(VI). Once Cr(VI) is formed it
can be released depending on the surface charge of Mn minerals
because Cr(VI) is mainly negatively charged in the form of HCrO4 −
[298].
Biogenic Mn oxides have a high sorption capacity for
metal(loid)s and also can oxidize metal(loid)s. Bacteria and fungi
enzymatically oxidize Mn(II) and produce insoluble Mn (III, IV)
oxides. Sorption of metal(loid)s by Mn oxides occurs by complexa-
tion above or below the structural vacancies and at structural sheet
edges, and incorporation into the vacancies by isomorphical sub-
stitution for Mn. Lead, Zn, Ni, and As(V) sorption and As(III) and
Cr(III) oxidation by biogenic Mn oxide produced by bacteria were
reported [299].
Nanosized metal oxides including ferric oxides, manganese
oxides, aluminum oxides, titanium oxides, magnesium oxides,
and cerium oxides are considered as promising adsorbents for
metal(loid) removal from the environment because of large surface
areas and high activities [300]. Nanosized alumina synthesized by
ammonium acetate fuel was effective in the adsorption of Pb, Ni,
and Zn from aqueous solutions. However, only a few studies applied
metal oxides in the immobilization of metal(loid)s in soil [301].
5.2.5. Biochar
Biochar has recently been applied as a novel carbonaceous mate-
rial to adsorb metal(loid)s in soil and water. Although, studies have
demonstrated the capability of biochar to serve as a green envi-
ronmental sorbent, one type of biochar may not be appropriate
for all cases of remediation. A number of variables are involved in
determining the exact role of a biochar for environmental manage-
ment. Pyrolysis condition and feedstock type are the main factors
influencing sorption behavior of biochars [302,303]. Even though
studies have shown the decrease of metal(loid)s like Cd, Cr, and
Pb in biochar-amended soils, investigations have revealed that
it could increase the mobility of some toxic metal(loid)s in soils
(Tables 2 and 3). Therefore, the examination of the biochar efficacy
on the mobility/stabilization of contaminants in multi-element
contaminated soils should be done. It is also important to predict
the metal(loid) stabilization mechanism of biochar to determine
the long-term effectiveness of the remediation technology.
Beesley et al. [144] applied hardwood-derived biochar to a
multi-element (As, Cu, Cd, and Zn) contaminated soil and observed
that while Cd and Zn were immobilized, Cu and As were mobi-
lized. Copper leaching was associated with high DOC contents at
the increased pH induced by biochar, whereas As leaching was
due to increase in soil pH to 7.56. Similarly, Park et al. [265]
154 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
reported Cu mobility in soil due to increased DOC with the addi-
tion of chicken manure-derived biochar. In contrast, the high pH
induced by biochar results in reduced solubility of Cd and Zn.
Increased mobility of As with biochar in soil was also noticed
by Hartley et al. [304]. Antimony also showed higher mobility in
soil treated with broiler litter-derived biochar [305]. The proba-
bility of electrostatic repulsion between anionic Sb and negatively
charged biochar surfaces resulted in desorption of Sb. Conversely,
Uchimiya et al. [306] suggested that the electrostatic attraction
between positively charged Cu and negatively charged biochar is
the prevailing mechanism of soil Cu immobilization. The Cu mobil-
ity/immobility is highly influenced by biochar organic C content.
Generally, the biochars produced at <500 ◦ C have high DOC con-
tent, which could facilitate the formation of soluble Cu complexes
with DOC, as reported by Beesley et al. [144] and Park et al. [265].
However, the biochars produced at high temperatures (>600 ◦ C) are
generally deficient in DOC, which could cause Cu immobilization in
soil [306].
The immobilization of Pb is, however, favored by biochars pro-
duced at low pyrolysis temperatures [305]. The increased release
of available P, K, and Ca from biochars produced at a low tem-
perature is associated with high Pb stabilization. Cao et al. [307]
demonstrated by X-ray diffraction (XRD) analysis that biochar
derived from dairy manure containing a high amount of avail-
able P immobilized Pb in shooting range soil by forming insoluble
hydroxypyromorphite (Pb5 (PO4 )3 (OH)). The role of O-containing
functional groups on biochar surfaces in metal(loid) binding was
predicted by Uchimiya et al. [308], who reported that cottonseed
hull-derived biochar produced at 350 ◦ C contains high oxygen con-
tent resulting in high uptake of Cu, Ni, Cd, and Pb.
Biochar has also demonstrated the potential to mitigate Cr
contaminated soils as they are highly reactive with many func-
tional groups and are able to donate electrons [37]. The increase in
proton supply for Cr(VI) reduction may be associated with the pres-
ence of several O-containing acidic (carbonyl, lactonic, carboxylic,
hydroxyl, and phenol) and basic (chromene, ketone, and pyrone)
functional groups [309,310]. The resulting Cr(III) either adsorbs
or participates in surface complexation with organic amendments
[81]. But, high pH biochars may prevent dissociation and oxidation
of phenolic and hydroxyl groups, which may limit the proton sup-
ply for reducing Cr(VI) [37]. Moreover, soil microbes can also reduce
Cr(VI) using C as an energy source from biochar [311]. Because of
the lower solubility of Cr(III) than Cr(VI), this reduction eventu-
ally results in immobilization of Cr, thereby reducing mobility and
transport [37].
6. Case studies
A large number of laboratory incubation and glasshouse exper-
iments have examined the effects of various mobilizing and
immobilizing amendments in the transformation and bioavailabil-
ity of heavy metal(oid)s in soils (Tables 2 and 3). However, only
a limited number of studies have examined the potential value of
these amendments in the remediation of metal(loid) contaminated
soils under field conditions. In this section, selected field experi-
ments in which the value of some of the soil amendments in the
remediation of various contaminated sites will be reported.
Inventory of field experiments on phytostabilization and
immobilization of metal(loid)s in Europe are summarized by Van-
gronsveld et al. [312]. By 2009, there were 27 field cases in 10
European countries documented in scientific publications. Soil
amendments, such as aluminosilicates and liming materials (zeo-
lites, beringite, lime, limestone, sugar beet lime, gravel sludge),
organic matter (biosolids compost, compost, peat, chicken manure)
and metal oxides (red mud, iron oxides, iron grit) were used to
immobilize As, Cd, Cu, Cr, Ni, Zn, Pb, Sb, thallium (Tl) in soils con-
taminated by industrial and agricultural activities. Plants used for
phytostabilization include Festuca rubra, Agrostis capillaris, Agrostis
castellana, Lolium perenne, Zea mays, Lactuca sativa, Betula pendula,
Alnus cordata, Crataegus monogyna, Salix caprea, Populus, Larix, Bras-
sica sp., Pistacia terebinthus, Cistus creticus, Pinus brutia, Bosea cypria,
and other grasses, vegetable crops, and trees [312].
The same study presents inventory of European field experi-
ments on phytoextraction, where 34 field cases are listed [312].
In nine cases, the addition of amendments, such as EDTA, nitrilo-
triacetic acid (NTA), citric acid, sulfur, nitrogen, and manure, were
used to increase phytoextraction efficiency of a number of plants
including Thlaspi caerulescens, Nicotiana tabacum, Brassica species,
H. annuus, Arabidopsis halleri, species of Salix, Populus, Alnus, Betula,
and many others.
A summary of pilot/field-scale demonstration projects imple-
mented in USA over the period 1982–2006 is given by Dermont
et al. [313]. The authors report 29 field scale cases where phy-
toremediation was used, 19 of them were phytoextraction, 4
phytostabilization, and 6 where both methods were used in combi-
nation. The targeted metal(loid)s in phytoextraction projects were
As, Cd, Cr, Cu, Hg, Pb, and Zn. The phytostabilization method was
applied to immobilize As, Cd, Cu, Ni, and Pb.
6.1. Case study 1: soil washing for cadmium contaminated paddy
soils
Soil washing is conventionally performed ex situ using appro-
priate equipment, in which extracting reagents are used to remove
hazardous metal(loid)s from soil into aqueous solution [314]. The
in situ soil washing is usually called “soil flushing”; therefore, the
word “soil washing” is consistently used in this section to avoid
confusion. The soil-washing techniques offer a great advantage of
high Cd-removal efficiency for contaminated soils. However, this
technique has been considered to be difficult to apply directly to
agricultural land, because wastewater drained during the process of
soil washing might pollute surrounding environments such as agri-
cultural canals, neighboring agricultural fields, and groundwater.
However, paddy fields possess an impervious hardpan just below
the subsurface layer, which hinders vertical movement of water.
The washed solution stays in the surface soil and does not pene-
trate into subsoil layers and groundwater. So, an in situ technology
of soil washing should be utilized fully to take advantage of such
unique characteristics of the paddy field.
The in situ soil-washing method of paddy fields has to meet the
following criteria [315,316]:
1. Use of washing chemicals with high efficiency of Cd removal, but
a minimal adverse impact on the paddy field and its surrounding
environment.
2. Cost-effective and environmentally sound operation of the sys-
tem.
3. Soil fertility of the paddy field and its crop growth are not greatly
affected by the washing treatment or can be easily corrected.
4. The effect of washing can last for a reasonably long period.
Makino and his team [315,316] have developed a new soil-
washing practice combined with on-site wastewater treatment
that completely satisfies the above mentioned four requirements,
which is discussed in the following sections.
Chelating agents, neutral salts, and strong acids have been
used for soil washing to solubilize metals. In particular, EDTA has
been commonly used due to its efficiency of Cd removal from
contaminated soils [317,318]. Ethylenediamine tetraacetic acid,
however, is a persistent chemical and stays for a long time in
the environment [319]. Some scientists, therefore, have used more
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166 155

Fig. 9. Portable purification system for the waste water drained from on-site soil washing [316].

biodegradable chelating agents instead of EDTA [319–322]. In cases wastewater as expected. The chloride concentration was less than
where biodegradable agents are used, however, the cost becomes 500 mg/L after water washing; this concentration is the threshold
relatively higher than the non-/less degradable counterparts. value for healthy rice crops. Soil washing considerably decreased
Makino et al. [315] noticed that calcium chloride (CaCl2 ) the Cd concentrations in the rice grain. The reduction rates of unpol-
is one of most appropriate soil-washing chemicals for Cd- ished rice after CaCl2 and FeCl3 washings were around 40 and 80%,
contaminated paddy soils on the basis of Cd-extraction efficiency, respectively. These results proved the efficiency and effectiveness
cost-effectiveness, and relatively low environmental impacts. The of the soil washing method for remediation of Cd-contaminated
high efficiency of CaCl2 in the extraction of soil Cd was mainly paddy fields.
attributable to the high selectivity of Ca for soil adsorption sites
compared with monovalent cations, the concurrent lowering of the 6.2. Case study 2: immobilization of copper and lead in mine spoil
solution pH due to hydrolysis of exchangeable Al, and the formation
of Cd–Cl complexes. Ferric chloride was found to be very effective in Acid drainage generation from sulfide containing mine wastes
the extraction of Cd in paddy soils [315]. The metal(loid) cation will causes soil acidification and contaminant leaching. A half ton acid
dissociate and form hydroxide precipitate. The driving force of the soil collected from a Cu ore transhipment station in the north
Cd extraction by FeCl3 is proton release coupled with the hydrol- of Sweden was stabilized with coal fly ash and peat, and along
ysis of ferric iron, which results in a sharp decrease in soil pH and with untreated soil, placed in outdoor lysimeters. The main aim
provides the optimal pH for Cd extraction [323]. Heavy metal(loid) of the study was to neutralize soil acidity and reduce leaching
solubilization was greatly enhanced by acidification and, at pH 1.3, of Cu and Pb. Leachates were collected for ten years. During the
reached more than 80% of the total Cd content of the soil [324]. first two years, the leaching of Cu and Pb decreased significantly
The soil-washing procedure developed by Makino et al. [316] in the treated soil while soil pH remained neutral [262]. The
consisted of three steps: (1) chemical washing with appropriate amendment combination also facilitated soil recovery through
chemical solutions, such as CaCl2 and FeCl3 to extract Cd from increased microbial biomass and respiration, soil enzyme activity,
soils; (2) followed by water washing to eliminate the remain- and sustained plant growth [325]. Further analyzes of leachates
ing chemicals; and (3) on-site treatment of the wastewater by a indicated that the immobilizing effect has been sustained during
portable purification apparatus with an alkali reaction chamber
and/or chelating material. In a field study, a part of the paddy field
was bound with plastic boards, which were partially buried on
the edges of the paddy field so that the upper two-thirds of each
board remained above the ground surface. This boundary provided
containment for additional water and chemicals in the paddy field.
The flushing chemical was applied to the bounded experimental
field, followed by addition of agricultural water, creating a soil-
solution ratio of 1:1.5–1:2. The soil suspension was mixed by a
tilling machine until it turned into slurry. The soil suspension was
allowed to rest after the mixing, and then the Cd-contained super-
natant of the slurry was drained off as wastewater and sent to the
wastewater treatment system [316] (Figs. 9 and 10).
The Cd concentrations in the treated wastewater were below
the Japanese environmental quality standard (0.01 mg Cd/L),
demonstrating that the in situ treatment system could treat the Fig. 10. Conceptual diagram of on-site soil washing [316].
156 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166

Cu_U Cu_T ssp. L.) (2004–2005), narrow leaf plantain (Plantago lanceolata L.)
100 (2006–2007), and velvet grass (Holcus lanatus L.) (2007–2008).
In 2004, the ammonium nitrate- (NH4 NO3 ) extractable Pb was
10
reduced by RM (90%), GS + RM (99%) and CA (99%). In 2007,
the NH4 NO3 -extractable Pb yielded similar results; however, the
mg/l

1
immobilization decreased in relation to the control because of
0.1 the deeper placement (from 15 to 25 cm), but the absolute values
remained below trigger values. Lead concentrations decreased by
0.01 RM (76%), GS + RM (97%), and CA (97%). It was assumed that those
reductions were mostly due to pH elevation and to a lesser extent
0.001 to the provided surface for fixation [327].
In barley, GS + RM reduced the grain Pb below the maximum
90
100
117
312
365
389
399
427
453
500
1038
1444
1589
1802
2128
2298
2516
2569
3236
permissible concentration (MPC) (0.22 mg/kg) in 2004 and 2005;
RM and CA reduced it (0.21 mg/kg) close to the MPC only in 2005.
time (days) Regarding plantain, Pb was not measured in 2006, but in 2007 the
shoot Pb was reduced far below MPC. In velvet grass, shoot Pb was
reduced by all treatments below the MPC in 2008. The treatments
Pb_U Pb_T elevated the pH up to 2 units in 2004 compared to the control. After
100 the deeper placement (2005) the difference was 1.5 units in 2007.
This was attributed to the dilution effect caused by the use of cir-
10 cular harrow for repeated mixing. The influence of the pH change
was found to be mostly responsible for the immobilizing mecha-
mg/l

1
nism, at least for a first fast sorption step on different surfaces from
clay minerals and Fe oxides [328]. Freisl-Hanl et al. [326] concluded
0.1
that the long-term efficiency of GS + RM seemed to be a realistic
4
0.01 and practical measure for extensively contaminated land, best in
combination with metal(loid)-excluding cultivars.
0.001
6.3. Case study 3: immobilization of arsenic in soil contaminated
90
100
117
312
365
389
399
427
453
500
1038
1444
1589
1802
2128
2298
2516
2569
3236

with wood impregnation chemicals

time (days) The ability of Fe-containing amendments to efficiently immo-

bilize As in soil is well known. However, Fe tends to immobilize
Fig. 11. Leaching of Pb and Cu in lysimeters with untreated soil (U) and soil treated
with coal fly ash and peat (T). Note logarithmic scale on y-axis [262]. unintended elements, such as nutrients, which further decreases
the soil capability to sustain vegetative growth and microbial func-
tions. Soil fertility and biological activity can be improved applying
the entire ten-years sampling period (Fig. 11). The fly ash was nutrient rich industrial residues (e.g., biosolids, compost) as co-
shown to have a long-term neutralizing capacity, as pH of the amendments [329–331]. The combination of soil amendments
treated soil remained neutral even after ten years (Fig. 12). should be carefully evaluated to keep soil pH and redox balance
Previous results from pot experiments by Freisl-Hanl et al. optimal for As immobilization. A two-year laboratory study was
[326] showed a high potential for the reduction of Pb entering the performed by Kumpiene et al. [332] where As-contaminated soil
food chain via crops grown on smelter-contaminated soils from was treated with Fe alone and in combination with coal fly ash,
Arnoldstein, Austria, by the use of amendments for immobiliza- biosolids from sewage sludge, peat, or gypsum. The aim of this study
tion. A field experiment was, therefore, optimized to look at the was to determine if the chemically stabilized As-contaminated
long-term efficiency of the treatments [lime (CA), red mud (RM), soil could be used as a construction material in the top layer of
gravel sludge + red mud (GS + RM)]. Field experiment results were a landfill cover. The As mobility and soil chemical and biochemical
obtained for five years. Besides soil and soil pore water samples, the properties were monitored for two years using 2 m columns repro-
following harvests were taken: spring barley (Hordeum distichon ducing the protection/vegetation layer of the landfill cover. The best
combination of soil amendments was Fe + peat, which reduced dis-
solved As in soil to the levels that are acceptable for drinking water
pH U pH T (0.01 mg/L). This soil showed the highest redox potential through-
8 out the entire 2 m columns, while in soil treated with Fe alone,
7 oxidizing conditions prevailed only in the top 0.5 m layer. Below
that, As mobility substantially increased. The Fe + peat amendment
6 combination was selected for a subsequent field experiment involv-
5 ing eight hundred tons of As contaminated soil. The soil was then
placed over an experimental landfill cell in the north of Sweden.
4
Untreated soil was used as the control. Analysis of leachates during
3 one season showed varying impact of soil treatment on As mobil-
2 ity depending on the water saturation of soil, which once again
highlights the importance of redox control in Fe-treated soils.
90
100
127
312
365
389
399
427
455
500
1038
1444
1589
1802
2128
2298
2516
2569
2853
2881
2896
2944
3236

6.4. Case study 4: immobilization of lead in smelter residue

time (days)

Fig. 12. Leachate pH from untreated soil (U) and soil treated with coal fly ash and A field study was undertaken by the In-Place Inactivation and
peat (T) [262]. Natural Ecological Restoration Technologies (IINERT) Soil-Metals
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Fig. 13. Influence of Pb speciation on Pb bioaccessibility. Linear combination fitting
results of Pb XAS results (A) of the control sample and soils treated with phosphoric
acid at 0.5% and 1% application rates. In vitro bioaccessibility results (B) at three
solution pHs of the control sample and soils treated with phosphoric acid at 0.5%
and 1% application rates [333].
Action Team aimed at developing and validating in situ techniques
as viable technologies for eliminating the hazards of Pb in soils and
surficial materials. Field plot demonstrations were established in a
residential setting adjacent to a Pb smelter, which operated from
the 1880s until its closing in the late 1960s at Joplin, MO, USA. The
amendments employed in the study were classified into three cat-
egories at varying concentrations: P only (triple super phosphate
(TSP), rock phosphate, and phosphoric acid), P and Fe (iron rich
residual (IRR) and TSP), and P and biosolids (biosolids and TSP).
Samples were collected at 3, 18, and 32 months after treatment
and evaluated for Pb immobilization as a function of time and
analyzed by in vivo animal feeding, in vitro chemical extraction,
and soil characterization via spectroscopic and extraction methods
[333–335].
For soil characterization, the soil samples were examined by X-
ray absorption spectroscopy (XAS) to determine Pb speciation, and
it was coupled with statistical analysis to quantify the Pb species
[333,334]. The speciation of Pb in the control soil included approx-
imately 35% organic matter associated Pb, 35% anglesite (PbSO4 ),
and 20% galena (PbS) as major components. The XAS results demon-
strated the formation of pyromorphite upon P addition (Fig. 13a).
157
A simplified in vitro extraction test designed to mimic the
human digestive system was employed [101] to examine the Pb
bioaccessibility in soil samples at solution pHs of 1.5, 2.0, and 2.5
[335]. Regardless of pH, the control soils were essentially identical
with Pb ranging from 58 to 60% bioaccessibility. The effect of the
amendment treatments was more pronounced when the in vitro
extracting solution was at a pH of 2.0 or 2.5, showing significant
reductions in Pb extractability in line with the speciation results
[334,335] (Fig. 13b).
Lastly, some of the soil samples were fed to swine, rat, and
human subjects to determine in vivo Pb bioavailability [333]. The
0.5% and 1.0% phosphoric acid treated soils at aging intervals of
3, 18, and 32 months showed statistically significant reductions in
blood lead levels in swine and rat. The human in vivo study utiliz-
ing methodology of Maddaloni et al. [336] found a 69% reduction in
Pb bioavailability for the 18 month 1% phosphoric acid treatment,
which was similar to the swine results.
7. Environmental implications of (im)mobilization
techniques
7.1. Leaching of contaminants
A number of issues need to be considered when using des-
orption and chelating agents to accelerate the remediation of
metal(loid) contaminated sites. The addition of these soil amend-
ments is likely to induce the solubilization of other than the
target metal(loid)s which may become phytotoxic (e.g., Al and
Mn). The increased solubilization of metal(loid)s can result in
their increased leaching to groundwater, especially in the absence
of active plant growth. Several column and lysimeter studies
have shown enhanced concentrations of heavy metal(loid)s in the
leachates following addition of synthetic chelates [132,337–339].
For example, Grčman et al. [340] found that while EDTA resulted in
an enhanced metal(loid) uptake by Brassica rapa, it also resulted in
leaching of Pb, Zn, and Cd. Similarly, Komárek et al. [341] observed
that EDDS concentrations at 3 and 6 mmol/kg enhanced the mobil-
ity (up to a 100-fold increase) and plant uptake of Cu (up to a 65-fold
increase), but they resulted in Cu leaching. Nevertheless, leaching in
the presence of the easily biodegradable chelant EDDS was found
to be significantly less than that for EDTA in small soil columns
[342]. Results by Ultra et al. [127] suggested that environmental
risks caused by the leaching of Cu and Cu-chelate, and the effect on
soil microbial activity, were less pronounced in the case of EDDS
addition than EDTA. The factors that influence EDDS degradation
include the dosage applied, soil properties, metal(loid) types, and
composition [343–347].
The extent of metal(loid) leaching during chelate-enhanced
phytoextraction is affected by a number of factors. These include
soil constituents and properties such as organic matter, amount and
type of clay, presence of carbonates, and pH [337,348,349], con-
centration of chelate applied [339,342], mode (split vs. full dose)
and time (before and after germination or just prior to harvest-
ing) of application [340,350], plant species [171,214], amount of
water applied [340], root zone processes [351], and extent by which
solubilized metal(loid)s are taken up by plants. For instance, the
application of EDTA prior to germination or just after germination,
when there is no or insignificant root mass to absorb metal(loid)s
from soil solution will significantly increase the risks of groundwa-
ter contamination.
Another important factor in chelate-induced phytoremedia-
tion is the stability of the metal–chelate complex with time. As
shown by Thayalakumaran et al. [124], EDTA application to a Cu-
contaminated soil resulted in an initial formation of the Cu–EDTA−
complex. Over time Cu–EDTA− reacted with soil Fe leading to the
158 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
formation of the more stable Fe(III)–EDTA− complex in the soil
solution, resulting in the release of Cu to soil solution and its re-
adsorption by the soil. Thayalakumaran et al. [348] demonstrated
the importance of time on the stability of the metal–chelate com-
plex in a pot experiment growing Agrostis tenuis. Numerous small
applications of EDTA resulted in a higher Cu accumulation in the
herbage compared with EDTA applied in one or two larger amounts.
Smolińska and Król [125] determined the extent of Hg leaching dur-
ing chemically assisted phytoextraction by EDTA, potassium iodide,
and citric acid. The leaching of Hg from contaminated soil was in the
range 39.4–44.1% depending on the time and the concentration of
Hg. Application of each of the chelators used during the experiment
increased the leaching of Hg from soil, the highest being noted in
which EDTA was used. Leaching of Hg from contaminated soil was
dependent on both Hg and chelator concentration.
There can be considerable variation in leaching of heavy
metal(loid)s during EDTA-assisted phytoextraction in soils varying
in calcium carbonate content. Sun et al. [337] evaluated leach-
ing of metal(loid)s (Cd, Cu, Pb, and Zn) after addition of 14 g
EDTA/kg to soils differing in calcium carbonate contents. Seven
days after EDTA application, Pb recovered in leachates was 3–30%
of the total Pb in soil. The amounts of metal(loid)s recovered in
leachates were reduced as the calcium carbonate content increased,
either due to the competition of Ca(II) to form Ca–EDTA complexes
[352] or precipitation of Pb in the form of PbCO3(s) (cerussite)
[353].
Alkaline hydrolysis of metal(loid)s with the chelating com-
pounds induces the formation of metal(loid) hydroxy precipitates.
Some of the chelating compounds are subjected to microbial degra-
dation, thereby affecting their long-term effectiveness. On the
contrary, the persistence of soluble EDTA–metal(loid) complexes
in soils can cause negative effects on soil microfauna. Ethylene-
diamine tetraacetic acid, DTPA, or ethylenediamine applied at
concentrations up to 3 mM were shown to inhibit nitrification rates
by disrupting and depleting the cellular stabilizing ions (Ca(II) and
Mg(II)) from nitrifying bacterial cells [354]. Application of EDTA at
10 mmol/kg inhibited the development of arbuscular mycorrhiza
and depressed the growth of soil fungi, bacteria, and actinomycetes
[340]. But Chen et al. [355] observed no negative effect on a micro-
bial community while studying chelate-assisted phytoremediation.
Many countries have banned or restricted the use of EDTA in
various products due to its inability to biodegrade in the environ-
ment and consequent risks for drinking water contamination. A
comprehensive research and monitoring of the aquatic environ-
ment in Germany has shown that EDTA can be detected in raw and
drinking waters of the entire territory of the country [356]. It is rea-
sonable to assume that similar situation might be found in many
other countries.
Phosphate amendments are being increasingly used for the
phytoremediation of As as desorbing agents, because P can dis-
place adsorbed As from soils and increase the solubility of As.
Davenport and Peryea [154] and Peryea [357] reported that P
fertilizer increased soil As availability to apple trees grown in As-
contaminated soils. This enhanced As release from the soil occurs
through competitive anion exchange which can potentially lead
to the increased As(V) leaching from soils [358]. Similarly, Codling
and Dao [359] noticed the leaching of As from the usage of potas-
sium phosphate in apple and plum orchard soils. Addition of P as
18% phosphorus pentoxide (7.2% P soluble in water) at a rate of
0.4% (w/w), revealed a 13-fold increase in leachable As compared to
untreated soil following the leaching test [304]. Thus, the increased
mobilization of As resulting from P input can result in its increased
leaching to groundwater, especially in the absence of active plant
growth. While Cao et al. [191] reported that P induced As uptake
by plants did not increase leaching, Caille et al. [360] observed that
P addition (50 mg P/kg soil) increased the As concentration in the
soil pore water without affecting the As concentration in the fronds
of Pteris vittata.
7.2. Long-term stability of immobilized metal(loid)s
It is important to know whether immobilized metal(loid)s are
reversible and stable enough not to be mobilized under natural
conditions for plants and microorganisms to take up [361]. Soil
environmental factors such as pH, redox potential, cation exchange
capacity, and organic matter content can affect metal(loid) mobil-
ity in soil. Especially, pH and redox conditions are the main factors
controlling the potential release of immobilized metal(loid)s to the
aqueous phase [362].
Soil organic amendments used to immobilize metal(loid)s are
subject to biodegradation. Degradation of organic amendment
applied in the remediation of metal(loid) contaminated soils influ-
ences the distribution of heavy metal(loid)s. Breakdown of organic
matter in the organic amendments may potentially increase the
bioavailability of metal(loid)s. However, mineralization can be
influenced by the extent of metal(loid) contamination, as microbial
population and activity decrease in the presence of toxic elements.
Binding of metal(loid)s to organic matter also may protect it from
biodegradation [363]. However, vegetation cover can keep supply-
ing organic matter and bind metal(loid)s in soil [364].
Microorganisms can immobilize metal(loid)s and the stability of
immobilized metal(loid)s varies under different physicochemical
conditions. The Pb and Cd bound as either silicates or oxyhydrox-
ides on the cell wall of Bacillus subtilis were stable, and Cd included
in bacterial-silicates was difficult to remobilize. However, decrease
of pH to 3.0 increased the release of Cd and Pb [365]. Cadmium
bound to fungal mycelia was remobilized by a filter-sterilized soil
extract and almost 100% of Cd was released at pH 4 [361].
Liming of soils to increase pH is another remediation method
requiring long-term monitoring. Liming is typically short-term gain
in terms of soil pH and over time will revert to the equilibrium of
the soil environment, which likely means a lower pH. Metal(loid)s
are very sensitive to changing pH conditions. Often organic soil
amendments provide a liming effect such as the case of lime com-
posted biosolids, which yield both organic matter degradation and
changing soil pH over time. Baker et al. [366] examined microbial
activity and plant growth on mine wastes enriched in Pb and Zn
amended with composted beef manure in the presence and absence
of lime and bentonite. Over a two year evaluation period with very
high compost addition (269 Mg/ha), there was an initial increase
in nutrient content, pH, water holding capacity, and enzyme activ-
ity; however, over time these attributes began to decline and they
were more notable at lower application rates (45 Mg/ha). While the
benefits may be short-lived, simple periodic amendment additions
may be all that is needed to sustain the immobilization process.
One important issue considering long-term efficiency of
metal(loid) immobilization using metal oxides is their sensitivity
to redox changes. At low redox conditions metal oxides become
unstable and bound contaminants tend to get released to soil solu-
tion [367]. When selecting metal oxides as soil amendments, it
is crucial to maintain good aeration of the soil profile to prevent
reductive dissolution of amendments and associated contaminants.
Pyromorphite type Pb mineral formed by P amendment is
known to be stable in most soils. Park et al. [281] reported that
rock phosphate treatment to immobilize Pb in soil was effective and
persistent for more than two years. However, speciation of Pb com-
pounds and quantification of the extent of Pb immobilization by
pyromorphite formation in P-amended soils have been difficult to
ascertain [335]. Questions have been raised on whether the immo-
bilized Pb by a P compound is stable in changing environmental
conditions. Lead–P precipitates can be dissolved in the presence
of soluble ligands such as cysteine, methionine, thiosulphate, and
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
Fig. 14. Structural dynamics of chloropyromorphite aged up to one year. Pb-LIII XAFS spectra (A) (raw data – solid line, fit data – dotted line), XRD patterns (B), HRTGA
derivative weight loss curves (C) of aged synthetic chloropyromorphite, and (D) relationship between aging time and derived first-order dissolution rate coefficients as
influenced by pH [369].
humic acid. Manecki et al. [368] tested the dissolution of pyromor-
phite in the presence of the trihydroxamate microbial siderophore
desferrioxamine-B as a function of pH, temperature, siderophore
concentration, and solution/solid ratios and showed that Pb was
released at pH 6–11 with the siderophore. Scheckel and Ryan [369]
demonstrated that dissolution of chloropyromorphite increased
with decreasing pH of the batch solution (Fig. 14). Similarly, Basta
et al. [370] showed that acidification of rock phosphate treated
soils to pH <6 resulted in phytotoxicity regardless of soil treatment
by increasing Cd and Zn. However, the stability and remobiliza-
tion of immobilized Pb in soil was not investigated and little work
has been done to evaluate the fate of the immobilized Pb. Ryan
et al. [333] examined P amended Pb soils up to 32 months after
treatment. They demonstrated increasing concentration of pyro-
morphite and reduced in vivo and in vitro bioavailability, but truly
long-term evaluations are non-existent. Fang et al. [371] tested the
stability of metal(loid)–P, especially the effect of planting. Plants
increased total Pb leaching even though dissolved Pb was reduced
by P treatments. Increase in total Pb leaching can be attributed to
the formation of colloids, which is facilitated by the increase of
leachate pH with planting.
Even though it is widely accepted that monitoring of long-
term stability of immobilized metal(loid)s is important, there are
a limited number of studies on the long-term stability of immobi-
lized metal(loid)s. Especially, remobilization of metal(loid)s with
breakdown of organic matter which binds metal(loid)s needs to
be investigated, particularly in acidic soils for metals. It cannot be
more clearly stated that immobilization remediation is not a “treat
159
and retreat” process and requires a long-term monitoring plan to
be successful.
8. Summary and conclusions
Since one of the primary objectives of remediating contami-
nated sites is to reduce the bioavailability of metal(loid)s, in situ
immobilization using some of the soil amendments that are low in
heavy metal(loid) content may offer a promising option. However,
a major inherent problem associated with immobilization tech-
niques is that, although the metal(loid)s become less bioavailable,
their total concentration in soils remains unchanged. The immo-
bilized metal(loid) may become plant available with time through
natural weathering process or through breakdown of high molecu-
lar weight organic–metal(loid) complexes. Although the formation
of soluble metal(loid)–organic complexes reduces the phytoavail-
ability of metal(loid)s, the mobility of the metal(loid) may be
facilitated greatly in soils receiving alkaline-stabilized biosolids
because of the reduction of metal(loid) adsorption and increased
concentration of soluble metal(loid)–organic complex in solution.
Soil amendments that are efficient in the mobilization of
metal(loid)s through desorption and chelation reactions can be
used to enhance bioavailability and subsequent removal through
plant uptake and soil washing. One of the problems with the
mobilization techniques is that in the absence of active plant
uptake the mobilized metal(loid)s are subject to leaching thereby
causing groundwater contamination. Furthermore, the mobilizing
amendments may not be specific to the target metal(loid), thereby
160 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
resulting in the release of phytotoxic metal(loid)s which inhibit
plant growth and subsequent removal of mobilized metal(loid)s.
Given the current knowledge on the mobilization and immobi-
lization techniques in relation to manipulating the bioavailability
of heavy metal(loid)s and subsequent remediation of contaminated
soils, the following research areas could be pursued:
– More studies are needed concerning the physiology of plants
treated with mobilizing or immobilizing agents. In the review by
Kirkham [118], 22 of the 38 papers included plants, and of these
22 papers only three considered the physiology of the plants
[135,372,373]. One paper considered uptake of metal(loid)s at
the biochemical level [374]. Madrid et al. [375] suggested areas
of future research dealing with chelate-assisted phytoremedia-
tion. More studies need to be done at the root–soil interface. The
studies need to include measurements of plant–water relations.
What are the effects of chelates on plant water potential, osmotic
potential, turgor potential, stomatal resistance, and transpiration
rate?
– More field studies are required to demonstrate the values of a
range of mobilizing and immobilizing soil amendments to reme-
diate contaminated soils. These field studies need to examine the
impact of amendments on co-contaminants. For example, addi-
tion of P compounds to a soil contaminated with both As and Pb
while facilitating the immobilization of Pb is likely to result in
the release of As.
– It is important to develop methods to demonstrate
(im)mobilization effectiveness. For example, use of advanced
spectroscopic methods can be used to investigate the in situ
short- and long-term effectiveness of (im)mobilization.
– Field studies should also be aimed at determining human
bioavailability, phytotoxicity, and ecoreceptor endpoints to show
reduction of risk resulting from soil amendments.
Acknowledgement
The postdoctoral fellowship program (PJ009219) with Dr. Won-
Il Kim at the National Academy of Agricultural Science, Rural
Development Administration, Republic of Korea, supported Dr.
Kunhikrishnan’s contribution.
References
[1] D.C. Adriano, Trace Elements in Terrestrial Environments: Biogeochemistry,
Bioavailability and Risks of Metals, second ed., Springer, New York, 2001.
[2] B. Knopf, H. König, Biomethylation of Heavy Metals in Soil and Terres-
trial Invertebrates: Soil Heavy Metals, Springer, Berlin/Heidelberg, 2010, pp.
315–328.
[3] S. Bhattacharya, K. Gupta, S. Debnath, U.C. Ghosh, D. Chattopadhyay, A.
Mukhopadhyay, Arsenic bioaccumulation in rice and edible plants and sub-
sequent transmission through food chain in Bengal basin: a review of the
perspectives for environmental health, Toxicol. Environ. Chem. 94 (2012)
429–441.
[4] P. Loganathan, M.J. Hedley, N.D. Grace, Pasture soils contaminated with fer-
tilizer derived cadmium and fluoride: livestock effects, Rev. Environ. Contam.
Toxicol. 192 (2008) 29–66.
[5] U. Pietrzak, N. Uren, Remedial options for copper-contaminated vineyard
soils, Soil Res. 49 (2011) 44–55.
[6] D.C. Adriano, W.W. Wenzel, J. Vangronsveld, N.S. Bolan, Role of assisted nat-
ural remediation in environmental cleanup, Geoderma 122 (2004) 121–142.
[7] J.H. Park, D. Lamb, P. Paneerselvam, G. Choppala, N. Bolan, J.-W. Chung, Role
of organic amendments on enhanced bioremediation of heavy metal (loid)
contaminated soils, J. Hazard. Mater. 185 (2011) 549–574.
[8] B.H. Robinson, G. Banuelos, H.M. Conesa, M.W.H. Evangelou, R. Schulin, The
phytomanagement of trace elements in soil, Crit. Rev. Plant Sci. 28 (2009)
240–266.
[9] D.T. Lamb, H. Ming, M. Megharaj, R. Naidu, Heavy metal (Cu, Zn Cd and Pb)
partitioning and bioaccessibility in uncontaminated and long-term contami-
nated soils, J. Hazard. Mater. 171 (2009) 1150–1158.
[10] R. Naidu, N.S. Bolan, Contaminant chemistry in soils: key concepts and
bioavailability, in: R. Naidu (Ed.), Chemical Bioavailability in Terrestrial Envi-
ronment, Elsevier, Amsterdam, The Netherlands, 2008, pp. 9–38.
[11] R. Naidu, R.S. Kookana, D.P. Oliver, S. Rogers, M.J. McLaughlin, Contaminants
and the Soil Environment in the Australasia–Pacific Region, Kluwer Academic
Publishers, London, 1996.
[12] N.S. Bolan, D.C. Adriano, R. Naidu, Role of phosphorus in (im)mobilization and
bioavailability of heavy metals in the soil–plant system, Rev. Environ. Contam.
Toxicol. 177 (2003) 1–44.
[13] J.N. Galloway, J.D. Thornton, S.A. Norton, H.I. Volchok, R.A.N. McLean, Trace-
metals in atmospheric deposition – a review and assessment, Atmos. Environ.
16 (1982) 1677–1700.
[14] C.W. Gray, R.G. McLaren, A.H.C. Roberts, Atmospheric accessions of heavy
metals to some New Zealand pastoral soils, Sci. Total Environ. 305 (2003)
105–115.
[15] J.E. Ferguson, J. Gavis, A review of the arsenic cycle in natural waters, Water
Res. 6 (1972) 1259–1274.
[16] S. Mahimairaja, N.S. Bolan, D. Adriano, B. Robinson, Arsenic contamination
and its risk management in complex environmental settings, Adv. Agron. 86
(2005) 1–82.
[17] H. Yan-Chu, Arsenic distribution in soils, in: J.O. Nriagu (Ed.), Arsenic in the
Environment: Part I. Cycling and Characterization, John Wiley & Sons Inc.,
New York, 1994, pp. 17–49.
[18] G. Yu, D. Sun, Y. Zheng, Health effects of exposure to natural arsenic in ground-
water and coal in China: an overview of occurrence, Environ. Health Perspect.
115 (2007) 636–642.
[19] M.A. Armienta, R. Rodriguez, O. Cruz, Arsenic content in hair of people exposed
to natural arsenic polluted groundwater at Zimapan, Mexico, Bull. Environ.
Contam. Toxicol. 59 (1997) 583–589.
[20] L.M. Del Razo, M.A. Arellano, M.E. Cebrian, The oxidation states of arsenic
in well-water from a chronic arsenicism area in northern Mexico, Environ.
Pollut. 64 (1990) 143–153.
[21] K.S. Dhillon, S.K. Dhillon, Quality of underground water and its contribu-
tion towards selenium enrichment of the soil–plant system for a seleniferous
region of northwest India, J. Hydrol. 272 (2003) 120–130.
[22] W.T. Frankenberger Jr., M. Arshad, Bioremediation of selenium contaminated
sediments and water, Biofactors 14 (2001) 241–254.
[23] J.C. Varekamp, P.R. Buseck, Global mercury flux from volcanic and geothermal
sources, Appl. Geochem. 1 (1986) 65–73.
[24] O. Lindqvist, K. Johansson, L. Bringmark, B. Timm, M. Aastrup, A. Andersson, G.
Hovsenius, L. Håkanson, Å. Iverfeldt, M. Meili, Mercury in the Swedish envi-
ronment – recent research on causes, consequences and corrective methods,
Water Air Soil Pollut. 55 (1991) xi–xi261.
[25] J. Fenger, Air pollution in the last 50 years – from local to global, Atmos.
Environ. 43 (2009) 13–22.
[26] R.J. Haynes, G. Murtaza, R. Naidu, Inorganic and organic constituents and
contaminants in biosolids: implications for land application, Adv. Agron. 104
(2009) 165–267.
[27] M.J. McLaughlin, K.G. Tiller, R. Naidu, D.P. Stevens, Review: the behaviour
and environmental impact of contaminants in fertilizers, Aust. J. Soil Res. 34
(1996) 1–54.
[28] R.A. Wuana, F.E. Okieimen, Heavy metals in contaminated soils: a review of
sources, chemistry, risks and best available strategies for remediation, ISRN
Ecol. 2011 (2011) 1–20.
[29] N.S. Bolan, M.A. Khan, J. Donaldson, D.C. Adriano, C. Matthew, Distribution
and bioavailability of copper in farm effluent, Sci. Total Environ. 309 (2003)
225–236.
[30] A.M. Wightwick, S.A. Salzman, S.M. Reichman, G. Allinson, N.W. Menzies,
Effects of copper fungicide residues on the microbial function of vineyard
soils, Environ. Sci. Pollut. Res. 20 (2013) 1574–1585.
[31] E. Chopin, B. Marin, R. Mkoungafoko, A. Rigaux, M. Hopgood, E. Delannoy,
B. Cancès, M. Laurain, Factors affecting distribution and mobility of trace ele-
ments (Cu, Pb Zn) in a perennial grapevine (Vitis vinifera L.) in the Champagne
region of France, Environ. Pollut. 156 (2008) 1092–1098.
[32] D.A. Heemsbergen, M.J. McLaughlin, M. Whatmuff, M.S.J. Warne, K. Broos,
M.J. Bell, D. Nash, G. Barry, D. Pritchard, N. Penney, Bioavailability of zinc and
copper in biosolids compared to their soluble salts, Environ. Pollut. 158 (2010)
1907–1915.
[33] A. Hildebrandt, M. Guillamón, S. Lacorte, R. Tauler, D. Barceló, Impact of pes-
ticides used in agriculture and vineyards to surface and groundwater quality
(North Spain), Water Res. 42 (2008) 3315–3326.
[34] A.M. Wightwick, S.A. Salzman, S.M. Reichman, G. Allinson, N.W. Menzies,
Inter-regional variability in environmental availability of fungicide derived
copper in vineyard soils: an Australian case study, J. Agric. Food Chem. 58
(2010) 449–457.
[35] M. van Zwieten, G. Stovold, L. van Zwieten, Alternatives to copper for disease
control in the Australian organic industry, A report for the Rural Indus-
tries Research and Development Corporation, RIRDC Publication No 07/110,
2007.
[36] X. Zhou, Z.L. He, Z.B. Liang, P.J. Stoffella, J. Fan, Y.G. Yang, C.A. Powell, Long-
term use of copper-containing fungicide affects microbial properties of citrus
grove soils, Soil Sci. Soc. Am. J. 75 (2011) 898–906.
[37] G.K. Choppala, N.S. Bolan, A. Kunhikrishnan, W. Skinner, B. Seshadri,
Concomitant reduction and immobilization of chromium in rela-
tion to its bioavailability in soils, Environ. Sci. Pollut. Res. (2013),
http://dx.doi.org/10.1007/s11356-013-1653-6 (in press).
[38] B. Robinson, M. Greven, S. Green, S. Sivakumaran, P. Davidson, B. Clothier,
Leaching of copper, chromium and arsenic from treated vineyard posts in
Marlborough, New Zealand, Sci. Total Environ. 364 (2006) 113–123.
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
[39] R. Schwer III, D.H. McNear, Chromated copper arsenate-treated fence posts in
the agronomic landscape: soil properties controlling arsenic speciation and
spatial distribution, J. Environ. Qual. 40 (2011) 1172–1181.
[40] N.S. Bolan, G. Choppala, A. Kunhikrishnan, J.H. Park, R. Naidu, Microbial
transformation of trace elements in soils in relation to bioavailability and
remediation, Rev. Environ. Contam. Toxicol. 225 (2013) 1–56.
[41] N.S. Bolan, R. Naidu, J.K. Syers, R.W. Tillman, Surface charge and solute inter-
actions in soils, Adv. Agron. 67 (1999) 88–141.
[42] D.L. Sparks, Environmental Soil Chemistry, second ed., Academic Press, San
Diego, 2003.
[43] H. Li, J. Wang, Y. Teng, Z. Wang, Study on the mechanism of transport of
heavy metals in soil in western suburb of Beijing, Chin. J. Geochem. 25 (2006)
173–177.
[44] G. Sposito, The Surface Chemistry of Soils, Oxford University Press, New York,
1984.
[45] M.D.C. Zenteno, R.C.A. de Freitas, R.B.A. Fernandes, M.P.F. Fontes, C.P. Jordão,
Sorption of cadmium in some soil amendments for in situ recovery of con-
taminated soils, Water Air Soil Pollut. 224 (2013) 1418–1426.
[46] N.S. Bolan, D.C. Adriano, P. Mani, A. Duraisamy, S. Arulmozhiselvan, Immobi-
lization and phytoavailability of cadmium in variable charge soils: I. Effect of
phosphate addition, Plant Soil 250 (2003) 83–94.
[47] R.D.R. Harter, R. Naidu, Role of metal–organic complexation in metal sorption
by soils, Adv. Agron. 55 (1995) 219–264.
[48] C.O. Hong, D.K. Lee, P.J. Kim, Feasibility of phosphate fertilizer to immobilize
cadmium in a field, Chemosphere 70 (2008) 2009–2015.
[49] C.O. Hong, D.Y. Chung, D.K. Lee, P.J. Kim, Comparison of phosphate materials
for immobilizing cadmium in soil, Arch. Environ. Contam. Toxicol. 58 (2010)
268–274.
[50] K. Lackovic, M.J. Angove, J.D. Wells, B.B. Johnson, Modeling the adsorption of
Cd(II) onto Muloorina illite and related clay minerals, J. Colloid Interface Sci.
257 (2003) 31–40.
[51] R. Naidu, N.S. Bolan, R.S. Kookana, K.G. Tiller, Ionic-strength and pH effects on
the adsorption of cadmium and the surface charge of soils, Eur. J. Soil Sci. 45
(1994) 419–429.
[52] E.R. Mouta, M.R. Soares, J.C. Casagrande, Copper adsorption as a function of
solution parameters of variable charge soils, J. Braz. Chem. Soc. 19 (2008)
996–1009.
[53] R.S. Stahl, B.R. James, Zinc sorption by B horizon soils as a function of pH, Soil
Sci. Soc. Am. J. 55 (1991) 1592–1597.
[54] R. Naidu, R.S. Kookana, M.E. Sumner, R.D. Harter, K.G. Tiller, Cadmium sorption
and transport in variable charge soils: a review, J. Environ. Qual. 26 (1997)
602–617.
[55] A. Nigussie, E. Kissi, M. Misganaw, G. Ambaw, Effect of biochar application
on soil properties and nutrient uptake of lettuces (Lactuca sativa) grown
in chromium polluted soils, Am. Eurasian J. Agric. Environ. Sci. 12 (2012)
369–376.
[56] L.M. Shuman, Effect of ionic strength and anions on zinc adsorption by two
soils, Soil Sci. Soc. Am. J. 50 (1986) 1438–1442.
[57] A. Violante, V. Cozzolino, L. Perelomov, A. Caporale, M. Pigna, Mobility and
bioavailability of heavy metals and metalloids in soil environments, J. Soil
Sci. Plant Nutr. 10 (2010) 268–292.
[58] N.S. Bolan, D.C. Adriano, A. Kunhikrishnan, T. James, R. McDowell, N. Sen-
esi, Dissolved organic carbon: biogeochemistry, dynamics and environmental
significance in soils, Adv. Agron. 110 (2011) 1–75.
[59] C.O. Hong, D.K. Lee, D.Y. Chung, P.J. Kim, Liming effects on cadmium stabiliza-
tion in upland soil affected by gold mining activity, Arch. Environ. Contam.
Toxicol. 52 (2007) 496–502.
[60] Y.S. Ok, S.E. Oh, M. Ahmad, S. Hyun, K.R. Kim, D.H. Moon, S.S. Lee, K.J. Lim, W.T.
Jeon, J.E. Yang, Effects of natural and calcined oyster shells on Cd and Pb immo-
bilization in contaminated soils, Environ. Earth Sci. 61 (2010) 1301–1308.
[61] S.L. McGowen, N.T. Basta, G.O. Brown, Use of diammonium phosphate to
reduce heavy metal solubility and transport in smelter-contaminated soil,
J. Environ. Qual. 30 (2001) 493–500.
[62] N.S. Bolan, S. Thiyagarajan, Retention, plant availability of chromium in soils
as affected by lime and organic amendments, Aust. J. Soil Res. 39 (2001)
1091–1103.
[63] P. Lu, N.T. Nuhfer, S. Kelly, Q. Li, H. Konishi, E. Elswick, C. Zhu, Lead coprecipi-
tation with iron oxyhydroxide nano-particles, Geochim. Cosmochim. Acta 75
(2011) 4547–4561.
[64] A. Violante, S. del Gaudio, M. Pigna, M. Ricciardella, D. Banerjee, Coprecipi-
tation of arsenate with metal oxides. 2. Nature mineralogy, and reactivity of
iron(III) precipitates, Environ. Sci. Technol. 41 (2007) 8275–8280.
[65] F. Cifuentes, W. Lindemann, L. Barton, Chromium sorption and reduction in
soil with implications to bioremediation, Soil Sci. 161 (1996) 233–241.
[66] T.E. Higgins, A. Halloran, M. Dobbins, A. Pittignano, In situ reduction of hex-
avalent chromium in alkaline soils enriched with chromite ore processing
residue, J. Air Waste Manage. Assoc. 48 (1998) 1100–1106.
[67] M. Banks, A. Schwab, C. Henderson, Leaching and reduction of chromium in
soil as affected by soil organic content and plants, Chemosphere 62 (2006)
255–264.
[68] J. Kumpiene, S. Ore, G. Renella, M. Mench, A. Lagerkvist, C. Maurice, Assess-
ment of zerovalent iron for stabilization of chromium copper, and arsenic in
soil, Environ. Pollut. 144 (2006) 62–69.
[69] D.V. Franco, L.M. Da Silva, W.F. Jardim, Chemical reduction of hexavalent
chromium present in contaminated soil using a packed bed column reactor,
Clean 37 (2009) 858–865.
161
[70] J.G.D. Kim, J.B. Chusuei, C.C. Deng, Oxidation of chromium(III) to (VI) by man-
ganese oxides, Soil Sci. Soc. Am. J. 66 (2002) 306–315.
[71] S.K. Porter, K.G. Scheckel, C.A. Impellitteri, J.A. Ryan, Toxic metals in the
environment: thermodynamic considerations for possible immobilisation
strategies for Pb, Cd, As, and Hg, Crit. Rev. Environ Sci. Technol. 34 (2004)
495–604.
[72] K. Amstaetter, T. Borch, P. Larese-Casanova, A. Kappler, Redox transformation
of arsenic by Fe(II)-activated goethite (␣-FeOOH), Environ. Sci. Technol. 44
(2010) 102–108.
[73] E.J. O’Loughlin, S.D. Kelly, K.M. Kemner, R. Csencsits, R.E. Cook, Reduction of
AgI , AuIII , CuII , and HgII by FeII /FeIII hydroxysulfate green rust, Chemosphere
53 (2003) 437–446.
[74] S.C.B. Myneni, T.K. Tokunaga, G.E. Brown Jr., Abiotic selenium redox transfor-
mations in the presence of Fe(II,III) oxides, Science 278 (1997) 1106–1109.
[75] P. Refait, L. Simon, J.M.R. Génin, Reduction of SeO4 2− anions and anoxic for-
mation of iron(II)–iron(III) hydroxy-selenate green rust, Environ. Sci. Technol.
34 (2000) 819–825.
[76] J. Olegario, N. Yee, M. Miller, J. Sczepaniak, B. Manning, Reduction of Se(VI)
to Se(-II) by zerovalent iron nanoparticle suspensions, J. Nanopart. Res. 12
(2010) 2057–2068.
[77] S.M. Ross, Retention transformation and mobility of toxic metals in soils, in:
S.M. Ross (Ed.), Toxic Metals in Soil–Plant Systems, Wiley, New York, 1994,
pp. 63–152.
[78] M.I. Madigan, T.D. Brock, Biology of Microorganisms, sixth ed., Prentice-Hall,
Englewood Cliffs, NJ, 1991, 874 pp.
[79] S.P. Bachate, R.M. Khapare, K.M. Kodam, Oxidation of arsenite by two ␤-
proteobacteria isolated from soil, Appl. Microbiol. Biotechnol. 93 (2012)
2135–2145.
[80] F. Battaglia-Brunet, M.C. Dictor, F. Garrido, C. Crouzet, D. Morin, K. Dekeyser,
M. Clarens, P. Baranger, An arsenic (III)-oxidizing bacterial population: selec-
tion, characterization, and performance in reactors, J. Appl. Microbiol. 93
(2002) 656–667.
[81] N.H. Hsu, S.L. Wang, Y.C. Lin, G.D. Sheng, J.F. Lee, Reduction of Cr(VI) by crop-
residue-derived black carbon, Environ. Sci. Technol. 43 (2009) 8801–8806.
[82] Y. Zhang, W.T. Frankenberger, Factors affecting removal of selenate in agri-
cultural drainage water utilizing rice straw, Sci. Total Environ. 305 (2003)
207–216.
[83] R.S. Oremland, J.T. Hollibaugh, A.S. Maest, T.S. Presser, L.G. Miller,
C.W. Culbertson, Selenate reduction to elemental selenium by anaero-
bic bacteria in sediments and culture: biogeochemical significance of a
novel sulfate-independent respiration, Appl. Environ. Microbiol. 55 (1989)
2333–2343.
[84] R.S. Oremland, M.J. Herbel, J.S. Blum, S. Langley, T.J. Beveridge, P.M. Ajayan,
T. Sutto, A.V. Ellis, S. Curran, Structural and spectral features of selenium
nanospheres produced by Se-respiring bacteria, Appl. Environ. Microbiol. 70
(2004) 52–60.
[85] H.A. Wiatrowski, P.M. Ward, T. Barkay, Novel reduction of mercury (II) by
mercury-sensitive dissimilatory metal reducing bacteria, Environ. Sci. Tech-
nol. 40 (2006) 6690–6696.
[86] W.T. Frankenberger, M.E. Losi, Application of bioremediation in the cleanup
of heavy elements and metalloids, in: H.D. Skipper, R.F. Turco (Eds.), Biore-
mediation: Science and Applications, Soil Science Special Publication No. 43,
Soil Science Society of America Inc., Madison, WI, USA, 1995, pp. 173–210.
[87] J.S. Thayer, F.E. Brinckman, The biological methylation of metals and metal-
loids, Adv. Organomet. Chem. 20 (1982) 313–356.
[88] L.L. Loseto, S.D. Siciliano, D.R.S. Lean, Methylmercury production in high Arctic
wetlands, Environ. Toxicol. Chem. 23 (2004) 17–23.
[89] M. Ravichandran, Interactions between mercury and dissolved organic matter
– a review, Chemosphere 55 (2004) 319–331.
[90] L. Lambertsson, M. Nilsson, Organic material: the primary control on mer-
cury methylation and ambient methyl mercury concentrations in estuarine
sediments, Environ. Sci. Technol. 40 (2006) 1822–1829.
[91] C.R. Lehr, Microbial methylation and volatilization of arsenic (PhD thesis),
Department of chemistry, The University of British Columbia, Canada, 2003.
[92] X.X. Yin, J. Chen, J. Qin, G.X. Sun, B.P. Rosen, Y.G. Zhu, Biotransformation and
volatilization of arsenic by three photosynthetic cyanobacteria, Plant Physiol.
156 (2011) 1631–1638.
[93] R.Y. Li, Y. Ago, W.J. Liu, N. Mitani, J. Feldmann, S.P. McGrath, J.F. Ma, F.J. Zhao,
The rice aquaporin Lsi1 mediates uptake of methylated arsenic species, Plant
Physiol. 150 (2009) 2071–2080.
[94] R. Rodríguez Martín-Doimeadios, E. Tessier, D. Amouroux, R. Guyoneaud,
R. Duran, P. Caumette, O. Donard, Mercury methylation/demethylation and
volatilization pathways in estuarine sediment slurries using species-specific
enriched stable isotopes, Mar. Chem. 90 (2004) 107–123.
[95] O. Regnell, A. Tunlid, Laboratory study of chemical speciation of mercury
in lake sediment and water under aerobic and anaerobic conditions, Appl.
Environ. Microbiol. 57 (1991) 789–795.
[96] S.M. Ullrich, T.W. Tanton, S.A. Abdrashitova, Mercury in the aquatic environ-
ment: a review of factors affecting methylation, Crit. Rev. Environ Sci. Technol.
31 (2001) 241–293.
[97] P.G.C. Campbell, in: A. Tessier, D.R. Turner (Eds.), Metal Speciation and
Bioavailability in Aquatic Systems, Wiley, New York, 1995.
[98] J. Vangronsveld, S.D. Cunningham, Introduction to the concepts, in: J.
Vangronsveld, S.D. Cunningham (Eds.), Metal Contaminated Soils: In-
Situ Inactivation and Phytorestoration, Springer-Verlag, Berlin, 1998, pp.
219–225.
162 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
[99] N.T. Basta, R. Gradwohl, Estimation of Cd, Pb, and Zn bioavailability in smelter-
contaminated soils by a sequential extraction procedure, J. Soil Contam. 9
(2000) 149–164.
[100] A. Khanmirzaei, K. Bazargan, A.A. Moezzi, B.K. Richards, K. Shahbazi, Sin-
gle and sequential extraction of cadmium in some highly calcareous soils
of Southwestern Iran, J. Soil Sci. Plant Nutr. 13 (2013) 153–164.
[101] M.V. Ruby, A. Davis, R. Schoof, S. Eberle, C.M. Sellstone, Estimation of bioavail-
ability using a physiologically based extraction test, Environ. Sci. Technol. 30
(1996) 420–430.
[102] X. Domene, S. Mattana, W. Ramírez, J. Colón, P. Jiménez, T. Balanyà, J.M.
Alcañiz, M. Bonmatí, Bioassays prove the suitability of mining debris mixed
with sewage sludge for land reclamation purposes, J. Soil. Sediment. 10 (2010)
30–44.
[103] J.E. Yang, E.O. Skogley, S.J. Georgitis, A.H. Ferguson, Phytoavailability soil
test: development and verification of theory, Soil Sci. Soc. Am. J. 55 (1991)
1358–1365.
[104] D. Bakircioglu, Y.B. Kurtulus, H. Íbar, Comparison of extraction procedures
for assessing soil metal bioavailability of to wheat grains, Clean 39 (2011)
728–734.
[105] M.E. Hodson, M.G. Vijver, W.J.G.M. Peijnenburg, Bioavailability in soils, in:
F.A. Swartjes (Ed.), Dealing with Contaminated Sites: From Theory Toward
Practical Application, Springer, Dordrecht, 2011, pp. 721–747.
[106] M.B. McBride, M. Pitiranggon, B. Kim, A comparison of tests for extractable
copper and zinc in metal-spiked and field-contaminated soil, Soil Sci. 174
(2009) 439–444.
[107] J.T. Sims, G.V. Johnson, Micronutrient soil test, in: J.J. Mortvedt (Ed.), Micronu-
trients in Agriculture, second ed., Soil Science Society of America, Madison,
WI, 1991, pp. 427–476.
[108] Q.H. Zhu, D.Y. Huang, S.L. Liu, Z.C. Luo, H.H. Zhu, B. Zhou, M. Lei, Z.X. Rao, X.L.
Cao, Assessment of single extraction methods for evaluating the immobiliza-
tion effect of amendments on cadmium in contaminated acidic paddy soil,
Plant Soil Environ. 58 (2012) 98–103.
[109] H.M. Zakir, N. Shikazono, Environmental mobility and geochemical partition-
ing of Fe, Mn, Co, Ni and Mo in sediments of an urban river, J. Environ. Chem.
Ecotoxicol. 3 (2011) 116–126.
[110] J. Abedin, P. Beckett, G. Spiers, An evaluation of extractants for assessment of
metal phytoavailability to guide reclamation practices in acidic soilscapes in
northern regions, Can. J. Soil Sci. 92 (2012) 253–268.
[111] J.W. Drexler, W.J. Brattin, An in vitro procedure for estimation of lead relative
bioavailability: with validation, Hum. Ecol. Risk Assess. 13 (2007) 383–401.
[112] I. Koch, K.J. Reimer, M.I. Bakker, N.T. Basta, M.R. Cave, S. Denys, M. Dodd,
B.A. Hale, R. Irwin, Y.W. Lowney, M.M. Moore, V. Paquin, P.E. Rasmussen, T.
Repaso-Subang, G.L. Stephenson, S.D. Siciliano, J. Wragg, G.J. Zagury, Vari-
ability of bioaccessibility results using seventeen different methods on a
standard reference material, NIST 2710, J. Environ. Sci. Health A 48 (2013)
641–655.
[113] J.C. Ng, A. Juhasz, E. Smith, R. Naidu, Assessing the bioavailability and
bioaccessibility of metals and metalloids, Environ. Sci. Pollut. Res. (2013),
http://dx.doi.org/10.1007/s11356-013-1820-9.
[114] C.U. Anyanwu, S.C. Nwankwo, A.N. Moneke, Soil bacterial response to intro-
duced metal stress, Int. J. Basic Appl. Sci. 11 (2011) 73–76.
[115] F.P. Zhang, C.F. Li, L.G. Tong, L.X. Yue, P. Li, Y.J. Ciren, C.G. Cao, Response of
microbial characteristics to heavy metal pollution of mining soils in central
Tibet, China, Appl. Soil Ecol. 45 (2010) 144–151.
[116] F. Amaro, A.P. Turkewitz, A. Martín-González, J.C. Gutiérrez, Whole-cell
biosensors for detection of heavy metal ions in environmental samples
based on metallothionein promoters from Tetrahymena thermophila, Microb.
Biotechnol. 4 (2011) 513–522.
[117] Å. Frostegård, A. Tunlid, E. Bååth, Use and misuse of PLFA measurements in
soils, Soil Biol. Biochem. 43 (2011) 1621–1625.
[118] M.B. Kirkham, Mobilizing and immobilizing materials for remediation of con-
taminated soils, in: Proceedings of the Twelfth International Conference on
the Biogeochemistry of Trace Elements, Athens, Georgia, June 16–20, 2013.
[119] A. Desaules, Critical evaluation of soil contamination assessment methods for
trace metals, Sci. Total Environ. 426 (2012) 120–131.
[120] M.B. McBride, Toxic metal accumulation from agricultural use of sludge: are
USEPA regulations protective? J. Environ. Qual. 24 (1995) 5–18.
[121] M.B. McBride, B. Hale, Molybdenum extractability in soils and uptake by
alfalfa 20 years after sewage sludge application, Soil Sci. 169 (2004) 505–514.
[122] M.B. McBride, B.K. Richards, T. Steenhuis, J.J. Russo, S. Sauve, Mobility and solu-
bility of toxic metals and nutrients in soil fifteen years after sludge application,
Soil Sci. 162 (1997) 487–500.
[123] M.B. McBride, B.K. Richards, T. Steenhuis, Bioavailability and crop uptake of
trace elements in soil columns amended with sewage sludge products, Plant
Soil 262 (2004) 71–84.
[124] Thayalakumaran, I. Vogeler, D.R. Scotter, H.J. Percival, B.H. Robinson, B.E.
Clothier, Leaching of copper from contaminated soil following the applica-
tion of EDTA. II. Intact core experiments and model testing, Aust. J. Soil Res.
41 (2003) 335–350.
[125] B. Smolińska, K. Król, Leaching of mercury during phytoextraction assisted by
EDTA, KI and citric acid, J. Chem. Technol. Biotechnol. 87 (2012) 1360–1365.
[126] M.B. Gabos, C.A. Abreu, A.R. Coscione, EDTA assisted phytoremediation of a
Pb contaminated soil: metal leaching and uptake by jack beans, Sci. Agric. 66
(2009) 506–514.
[127] U. Ultra Jr., A. Yano, K. Iwasaki, S. Tanaka, Y. Kang, K. Sakurai, Influence of
chelating agent addition on copper distribution and microbial activity in soil
and copper uptake by brown mustard (Brassica juncea), Soil Sci. Plant Nutr.
51 (2005) 193–202.
[128] T.M. Zeremski-Škorić, P.Ð. Sekulić, I.V. Maksimović, S.I. Šeremešić, J.M.
Ninkov, S.B. Milić, J.R. Vasin, Chelate-assisted phytoextraction: effect of EDTA
and EDDS on copper uptake by Brassica napus L., J. Serb. Chem. Soc. 75 (2010)
1279–1289.
[129] A. Cao, A. Carucci, T. Lai, P.L. Colla, E. Tamburini, Effect of biodegradable chelat-
ing agents on heavy metals phytoextraction with Mirabilis jalapa and on its
associated bacteria, Eur. J. Soil Biol. 43 (2007) 200–206.
[130] Y.B. Sun, Q.X. Zhou, J. An, W.T. Liu, R. Liu, Chelator-enhanced phytoextraction
of heavy metals from contaminated soil irrigated by industrial wastewa-
ter with the hyperaccumulator plant (Sedum alfredii Hance), Geoderma 150
(2009) 106–112.
[131] A. Karczewska, K. Orlow, C. Kabala, K. Szopka, B. Galka, Effects of chelat-
ing compounds on mobilization and phytoextraction of copper and lead in
contaminated soils, Commun. Soil Sci. Plant Anal. 42 (2011) 1379–1389.
[132] A.G. Wang, C.L. Luo, R.X. Yang, Y.H. Chen, Z.G. Shen, X.D. Li, Metal leaching
along soil profiles after the EDDS application – a field study, Environ. Pollut.
164 (2012) 204–210.
[133] Y.A. Almaroai, A.R.A. Usman, M. Ahmad, K.R. Kim, M. Vithanage, Y.S. Ok, Role of
chelating agents on release kinetics of metals and their uptake by maize from
chromated copper arsenate contaminated soil, Environ. Technol. 34 (2013)
747–755.
[134] L. Jean-Soro, F. Bordas, J.C. Bollinger, Column leaching of chromium and nickel
from a contaminated soil using EDTA and citric acid, Environ. Pollut. 165
(2012) 175–181.
[135] Y. Gao, C. Miao, J. Xia, C. Luo, L. Mao, P. Zhou, W. Shi, Effect of citric acid on
phytoextraction and antioxidative defense in Solanum nigrum L. as a hyperac-
cumulator under Cd and Pb combined pollution, Environ. Earth Sci. 65 (2012)
1923–1932.
[136] T. Veselý, P. Tlustoš, J. Száková, Organic acid enhanced soil risk element (Cd,
Pb and Zn) leaching and secondary bioconcentration in water lettuce (Pistia
stratiotes L.) in the rhizofiltration process, Int. J. Phytoremediation 14 (2012)
335–349.
[137] M.W.H. Evangelou, H. Daghan, A. Schaeffer, The influence of humic acids on
the phytoextraction of cadmium from soil, Chemosphere 57 (2004) 207–213.
[138] H. Li, Q. Wang, Y. Cui, Y. Dong, P. Christie, Slow release chelate enhancement
of lead phytoextraction by corn (Zea mays L.) from contaminated soil – a
preliminary study, Sci. Total Environ. 339 (2005) 179–187.
[139] K.K. Chiu, Z.H. Ye, M.H. Wong, Enhanced uptake of As, Zn, and Cu by Vetive-
ria zizanioides and Zea mays using chelating agents, Chemosphere 60 (2005)
1365–1375.
[140] E. Reinoso-Maset, P.J. Worsfolrd, M.J. Keith-Roach, The effect of EDTA, NTA
and picolinic acid on Th(IV) mobility in a ternary system with natural sand,
Environ. Pollut. 162 (2012) 399–405.
[141] A. Esringü, M. Turan, The roles of diethylenetriamine pentaacetate (DTPA) and
ethylenediamine disuccinate (EDDS) in remediation of selenium from con-
taminated soil by Brussels sprouts (Brassica oleracea var. gemmifera), Water
Air Soil Pollut. 223 (2012) 351–362.
[142] A. Hanč, P. Tlustoš, J. Száková, J. Habart, K. Gondek, Direct and subsequent
effect of compost and poultry manure on the bioavailability of cadmium
and copper and their uptake by oat biomass, Plant Soil Environ. 54 (2008)
271–278.
[143] L. Wu, Z. Li, I. Akahane, L. Liu, C. Han, T. Makino, Y. Luo, P. Christie, Effects of
organic amendments on Cd, Zn and Cu bioavailability in soil with repeated
phytoremediation by Sedum plumbizincicola, Int. J. Phytoremediation 14
(2012) 1024–1038.
[144] L. Beesley, E. Moreno-Jiménez, J.L. Gomez-Eyles, Effects of biochar and green-
waste compost amendments on mobility, bioavailability and toxicity of
inorganic and organic contaminants in a multi-element polluted soil, Environ.
Pollut. 158 (2010) 2282–2287.
[145] L. Beesley, M. Marmiroli, L. Pagano, V. Pigoni, G. Fellet, T. Fresno, T. Vamer-
ali, M. Bandiera, N. Marmiroli, Biochar addition to an arsenic contaminated
soil increases arsenic concentrations in the pore water but reduces uptake to
tomato plants (Solanum lycopersicum L.), Sci. Total Environ. 454–455 (2013)
598–603.
[146] A. Méndez, A. Gómez, J. Paz-Ferreiro, G. Gascó, Effects of sewage sludge
biochar on plant metal availability after application to a Mediterranean soil,
Chemosphere 89 (2012) 1354–1359.
[147] L.S. Forsberg, D.B. Kleja, M. Greger, S. Ledin, Effects of sewage sludge on solu-
tion chemistry and plant uptake of Cu in sulphide mine tailings at different
weathering stages, Appl. Geochem. 24 (2009) 475–482.
[148] R.P. Singh, M. Agrawal, Effect of different sewage sludge applications on
growth and yield of Vigna radiata L. field crop: metal uptake by plant, Ecol.
Eng. 36 (2010) 969–972.
[149] R.P. Singh, M. Agrawal, Effects of sewage sludge amendment on heavy metal
accumulation and consequent responses of Beta vulgaris plants, Chemosphere
67 (2007) 2229–2240.
[150] H. Kandil, M.I. El-Kherbawy, S. Ibrahim, A. Abd-Elfattah, M.R. Abd El-Moez,
S.H. Badawy, Effect of different sources and rates of some organic manure on
content of some heavy metals in different soils and plants grown therein: II.
Effect on corn plants, Soil Form. Fact. Proc. Temp. Zone 11 (2012) 19–32.
[151] A. Izhevska, The impact of manure, municipal sewage sludge and compost
prepared from municipal sewage sludge on crop yield and content of Mn,
Zn, Cu, Ni, Pb, Cd in spring rape and spring triticale, J. Elem. 14 (2009)
449–456.
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
[152] M.T. Aide, M.F. Cummings, The influence of pH and phosphorus on the adsorp-
tion of chromium (VI) on boehmite, Soil Sci. 162 (1997) 599–603.
[153] M.G.M. Alam, S. Tokunaga, F. Stagnitti, Removal of arsenic from contami-
nated soils using different salt extractants, J. Environ. Sci. Health A 42 (2007)
447–451.
[154] J.R. Davenport, F.J. Peryea, Phosphate fertilizers influence leaching of lead and
arsenic in soil contaminated with lead arsenate, Water Air Soil Pollut. 57–58
(1991) 101–110.
[155] B.R. James, J.C. Petura, R.J. Vitale, G.R. Mussoline, Hexavalent chromium
extraction from soils: a comparison of five methods, Environ. Sci. Technol.
29 (1995) 2377–2381.
[156] F.J. Peryea, Phosphate-induced release of arsenic from soils contaminated
with lead arsenate, Soil Sci. Soc. Am. J. 55 (1991) 1301–1306.
[157] M. Zupančič, S. Lavrič, P. Bukovec, Metal immobilization and phosphorus
leaching after stabilization of pyrite ash contaminated soil by phosphate
amendments, J. Environ. Monit. 14 (2012) 704–710.
[158] J.C. Seaman, J.S. Arey, P.M. Bertsch, Immobilization of nickel and other metals
in contaminated sediments by hydroxyapatite addition, J. Environ. Qual. 30
(2001) 460–469.
[159] N.N.J. Barrow, On the displacement of adsorbed anions from soil. 1. Displace-
ment of molybdenum by phosphate and by hydroxide, Soil Sci. 116 (1973)
423–431.
[160] R.J. Bartlett, J.M. Kimble, Behavior of chromium in soils: II. Hexavalent forms,
J. Environ. Qual. 5 (1976) 383–386.
[161] A. Karczewska, K. Kocan, D. Tyma, B. Galka, Effects of phosphorus and iron
compounds on arsenic uptake by selected vegetable species from soils pol-
luted with this element, Fresenius Environ. Bull. 18 (2009) 1975–1980.
[162] E. Smith, R. Naidu, A.M. Alston, Chemistry of arsenic in soils: II. Effect of pH
and ionic strength, J. Environ. Qual. 31 (2002) 137–143.
[163] S. Goldberg, Competitive adsorption of molybdenum in the presence of phos-
phorus or sulfur on gibbsite, Soil Sci. 175 (2010) 105–110.
[164] R.J. Xie, A.F. Mackenzie, Z.J. Lou, Causal-modeling pH and phosphate effects
on molybdate sorption in 3 temperate soils, Soil Sci. 155 (1993) 385–397.
[165] C. Neunhauserer, M. Berreck, H. Insam, Remediation of soils contaminated
with molybdenum using soil amendments and phytoremediation, Water Air
Soil Pollut. 128 (2001) 85–96.
[166] A.A. Meharg, M.R. Macnair, Suppression of the high affinity phosphate uptake
system: a mechanism of arsenate tolerance in Holcus lanatus L., J. Exp. Bot. 43
(1992) 519–524.
[167] M. Lei, X. Wan, Z. Huang, T. Chen, X. Li, Y. Li, First evidence on different
transportation modes of arsenic and phosphorus in arsenic hyperaccumulator
Pteris vittata, Environ. Pollut. 161 (2012) 1–7.
[168] M. Pigna, V. Cozzolino, A. Violante, A.A. Meharg, Influence of phosphate on the
arsenic uptake by wheat (Triticum durum L.) irrigated with arsenic solutions
at three different concentrations, Water Air Soil Pollut. 197 (2009) 371–380.
[169] P. Ravenscroft, J. McArthur, B. Hoque, Geochemical and palaeohydrological
controls on pollution of groundwater by arsenic, in: W.R. Chappell, C.O. Aber-
nathy, R. Calderon (Eds.), Arsenic Exposure and Health Effects, IV, Elsevier
Science Ltd., Oxford, 2001, pp. 53–77.
[170] N.S. Bolan, S. Mahimairaja, A. Kunhikrishnan, B. Seshadri, R. Thangara-
jan, Bioavailability and ecotoxicity of arsenic in solution culture and soil
system: implications to remediation, Environ. Sci. Pollut. Res. (2013),
http://dx.doi.org/10.1007/s11356-013-1827-2 (in press).
[171] Y.H. Chen, X.D. Li, Z.G. Shen, Leaching and uptake of heavy metals by ten
different species of plants during an EDTA-assisted phytoextraction process,
Chemosphere 57 (2004) 187–196.
[172] F.N. Moreno, C.W.N. Anderson, R.B. Stewart, B.H. Robinson, M. Ghomshei,
J.A. Meech, Induced plant uptake and transport of mercury in the pres-
ence of sulphur-containing ligands and humic acids, New Phytol. 166 (2005)
445–454.
[173] F.N. Moreno, C.W.N. Anderson, R.B. Stewart, B.H. Robinson, Mercury volatil-
isation and phytoextraction from base metal mine tailings, Environ. Pollut.
136 (2005) 341–352.
[174] S.P. Bizily, C.L. Rugh, A.O. Summers, R.B. Meagher, Phytoremediation of methyl
mercury pollution: MerB expression in Arabdopsis thaliana confers resistance
to organomercurials, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6808–6813.
[175] S. Lyyra, R.B. Meagher, T. Kim, A. Heaton, P. Montello, R.S. Balish, S.A. Merkle,
Coupling two mercury resistance genes in Eastern cottonwood enhances the
processing of organomercury, Plant Biotechnol. J. 5 (2007) 254–262.
[176] C.L. Rugh, H.D. Wilde, N.M. Stacks, D.M. Thompson, A.O. Summers, R.B.
Meagher, Mercury ion reduction and resistance in transgenic Arabdopsis
thaliana plants expressing a modified bacterial merA gene, Proc. Natl. Acad.
Sci. U.S.A. 93 (1996) 3182–3187.
[177] M.B. Kirkham, EDTA-facilitated phytoremediation of soil with heavy metals
from sewage sludge, Int. J. Phytoremediation 2 (2000) 159–172.
[178] M.S. Liphadzi, M.B. Kirkham, Chelate-assisted heavy metal removal by sun-
flower to improve soil with sludge, J. Crop Improv. 16 (2006) 153–172.
[179] M.S. Liphadzi, M.B. Kirkham, Heavy-metal displacement in chelate-treated
soil with sludge during phytoremediation, J. Plant Nutr. Soil Sci. 169 (2006)
737–744.
[180] M.S. Liphadzi, M.B. Kirkham, Partitioning and accumulation of heavy metals
in sunflower grown at biosolids farm in EDTA-facilitated phytoremediation,
Biorem. Biodiv. Bioavail. 3 (2009) 36–42.
[181] M.S. Liphadzi, M.B. Kirkham, K.R. Mankin, G.M. Paulsen, EDTA-assisted heavy-
metal uptake by poplar and sunflower grown at a long-term sewage-sludge
farm, Plant Soil 257 (2003) 171–182.
163
[182] M.S. Liphadzi, M.B. Kirkham, G.M. Paulsen, Auxin-enhanced root growth
for phytoremediation of sewage-sludge amended soil, Environ. Technol. 27
(2006) 695–704.
[183] P. Alvarenga, A.P. Goncalves, R.M. Fernandes, A. Varennes, G. Vallini, E. Duarte,
Organic residues as immobilizing agents in aided phytostabilization: (I)
effects on soil chemical characteristics, Chemosphere 74 (2009) 1292–1300.
[184] R. O’Dell, W. Silk, P. Green, V. Claassen, Compost amendment of Cu–Zn mine
spoil reduced toxic bioavailable heavy metal concentrations and promotes
establishment and biomass production of Bromus carinatus (Hook and Arn.),
Environ. Pollut. 148 (2007) 115–124.
[185] Q.J. Song, G.M. Greenway, A study of the elemental leachability and retention
capability of compost, J. Environ. Monit. 6 (2004) 31–37.
[186] D.J. Walker, R. Clemente, M.P. Bernal, Contrasting effects of manure and com-
post on soil pH, heavy metal availability and growth of Chenopodium album
L. in a soil contaminated by pyritic mine waste, Chemosphere 57 (2004)
215–224.
[187] M.P. Bernal, R. Clemente, D.J. Walker, The role of organic amendments in the
bioremediation of heavy metal-polluted soils, in: R.W. Gore (Ed.), Environ-
mental Research at the Leading Edge, Nova Science Publishers Inc., New York,
2007, pp. 1–57.
[188] L.M. Shuman, Effect of organic waste amendments on zinc adsorption by two
soils, Soil Sci. 164 (1999) 197–205.
[189] D.J. Walker, R. Clemente, A. Roig, M.P. Bernal, The effect of soil amendments
on heavy metal bioavailability in two contaminated Mediterranean soils, Env-
iron. Pollut. 22 (2003) 303–312.
[190] R. Clemente, W. Hartley, P. Riby, N.M. Dickinson, N.W. Lepp, Trace element
mobility in a contaminated soil two years after field-amendment with a green
waste compost mulch, Environ. Pollut. 158 (2010) 1644–1651.
[191] X. Cao, L.Q. Ma, A. Shiralipour, Effects of compost and phosphate amendments
on arsenic mobility in soils and arsenic uptake by the hyperaccumulator, Pteris
vittata L., Environ. Pollut. 126 (2003) 157–167.
[192] W. Hartley, N.M. Dickinson, P. Riby, E. Leese, J. Morton, N.W. Lepp, Arsenic
mobility and speciation in a contaminated urban soil are affected by differ-
ent methods of green waste compost application, Environ. Pollut. 158 (2010)
3560–3570.
[193] M. Mench, S. Bussière, J. Boisson, E. Castaing, J. Vangronsveld, A. Ruttens, T.
De Koe, P. Bleeker, A. Assunção, A. Manceau, Progress in remediation and
revegetation of the barren Jales gold mine spoil after in situ treatments, Plant
Soil 249 (2003) 187–202.
[194] A.D. Redman, D. Macalady, D. Ahmann, Natural organic matter affects arsenic
speciation and sorption onto hematite, Environ. Sci. Technol. 36 (2002)
2889–2896.
[195] L. Beesley, N. Dickinson, Carbon and trace element mobility in an urban soil
amended with green waste compost, J. Soil. Sediment. 10 (2010) 215–222.
[196] D. Businelli, L. Massaccesi, D. Said-Pullicino, G. Gigliotti, Long-term distribu-
tion, mobility and plant availability of compost-derived heavy metals in a
landfill covering soil, Sci. Total Environ. 407 (2009) 1426–1435.
[197] A. Kunhikrishnan, N.S. Bolan, K. Müller, S. Laurenson, R. Naidu, W.I. Kim, The
influence of wastewater irrigation on the transformation and bioavailability
of heavy metal(loid)s in soil, Adv. Agron. 115 (2012) 215–297.
[198] S. Wang, C.N. Mulligan, Effect of natural organic matter on arsenic release from
soil and sediments into groundwater, Environ. Geochem. Health 28 (2006)
197–214.
[199] X.D. Cao, L.Q. Ma, Effects of compost and phosphate on plant arsenic accu-
mulation from soils near pressure-treated wood, Environ. Pollut. 132 (2004)
435–442.
[200] A. Perez-de-Mora, P. Burgos, F. Cabrera, E. Madejon, In situ amendments and
revegetation reduce trace element leaching in a contaminated soil, Water Air
Soil Pollut. 185 (2007) 209–222.
[201] H. Xu, B. Allard, A. Grimvall, Effects of acidification and natural organic materi-
als on the mobility of arsenic in the environment, Water Air Soil Pollut. 57–58
(1991) 269–278.
[202] R. Flynn, A.L. Ulery, Y. Lamm, Compost-enhanced remediation of arsenic- and
lead-contaminated soil, in: Presented to the Western Nutrient Management
Conference, Salt Lake City, March 8–9, 2001.
[203] E. Moreno-Jiménez, R. Clemente, A. Mestrot, A.A. Meharg, Arsenic and sele-
nium mobilisation from organic matter treated mine spoil with and without
inorganic fertilisation, Environ. Pollut. 173 (2013) 238–244.
[204] M. Fleming, Y. Tai, P. Zhuang, M.B. McBride, Extractability and bioavailability
of Pb and As in historically contaminated orchard soil: effects of compost
amendments, Environ. Pollut. 177 (2013) 90–97.
[205] M. Udovic, M.B. McBride, Influence of compost addition on lead and arsenic
bioavailability in reclaimed orchard soil assessed using Porcellio scaber bioac-
cumulation test, J. Hazard. Mater. 205–206 (2012) 144–149.
[206] L. Beesley, M. Marmiroli, The immobilisation and retention of soluble arsenic,
cadmium and zinc by biochar, Environ. Pollut. 159 (2011) 474–480.
[207] F.Y. Wang, Z.Y. Shi, X.F. Xu, X.G. Wang, Y.J. Li, Contribution of AM inoculation
and cattle manure to lead and cadmium phytoremediation by tobacco plants,
Environ. Sci. Process Impacts 15 (2013) 794–801.
[208] D. Houben, L. Evrard, P. Sonnet, Mobility, bioavailability and
pH-dependent leaching of cadmium, zinc and lead in a con-
taminated soil amended with biochar, Chemosphere (2013),
http://dx.doi.org/10.1016/j.chemosphere.2013.03.055 (in press).
[209] L.M. Shuman, Effect of organic waste amendments on cadmium and lead
in soil fractions of two soils, Commun. Soil Sci. Plant Anal. 29 (1998)
2939–2952.
164 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
[210] N.C. Munksgaard, B.G. Lottermoser, K. Blake, Prolonged testing of metal mobil-
ity in mining-impacted soils amended with phosphate fertilizers, Water Air
Soil Pollut. 223 (2012) 2237–2255.
[211] P. Tanhan, P. Pokethitiyook, M. Kruatrachue, R. Chaiyarat, S. Upatham, Effects
of soil amendments and EDTA on lead uptake by Chromolaena odorata: green-
house and field trial experiments, Int. J. Phytoremediation 13 (2011) 897–911.
[212] T. Lambrechts, Q. Gustot, E. Couder, D. Houben, A. Iserentant, S. Lutts, Com-
parison of EDTA-enhanced phytoextraction and phytostabilisation strategies
with Lolium perenne on a heavy metal contaminated soil, Chemosphere 85
(2011) 1290–1298.
[213] R.W. Neugschwandtner, P. Tlustoš, M. Komárek, J. Száková, L. Jakoubková,
Chemically enhanced phytoextraction of risk elements from a contaminated
agricultural soil using Zea mays and Triticum aestivum: performance and metal
mobilization over a three year period, Int. J. Phytoremediation 14 (2012)
754–771.
[214] F. Madrid, M.S. Liphadzi, M.B. Kirkham, Heavy metal displacement in chelate-
irrigated soil during phytoremediation, J. Hydrol. 272 (2003) 107–119.
[215] M.S. Liphadzi, M.B. Kirkham, Availability of heavy metals in soil with injected
sludge and composted-sludge soil, Adv. Geoecol. 38 (2006) 203–214.
[216] I.H. Wahla, M.B. Kirkham, Heavy metal displacement in salt-water-irrigated
soil during phytoremediation, Environ. Pollut. 155 (2008) 271–283.
[217] M. Alexander, Biodegradation, Bioremediation, second ed., Academic Press,
San Diego, CA, 1999.
[218] G.M. Gadd, Bioremedial potential of microbial mechanisms of metal mobi-
lization and immobilization, Curr. Opin. Biotechnol. 11 (2000) 271–279.
[219] S.L. Chen, D.B. Wilson, Genetic engineering of bacteria and their potential for
Hg2+ bioremediation, Biodegradation 8 (1997) 97–103.
[220] U. Krämer, I.N. Talke, M. Hanikenne, Transition metal transport, FEBS Lett. 581
(2007) 2263–2272.
[221] N.S. Bolan, S. Mahimairaja, M. Megharaj, R. Naidu, D.C. Adriano, Biotrans-
formation of arsenic in soil and aquatic environments: bioavailability and
bioremediation, in: R. Naidu, E. Smith, G. Owens, P. Bhattacharya, P. Nade-
baum (Eds.), Managing Arsenic in the Environment: from Soil to Human
Health, CSIRO, Australia, 2006, pp. 433–453.
[222] E.A. Perpetuo, C.B. Souza, C.A.O. Nascimento, Engineering bacteria for biore-
mediation, in: A. Carpi (Ed.), Progress in Molecular and Environmental
Bioengineering from Analysis and Modeling to Technology Applications,
InTech Publishers, 2011, pp. 605–632.
[223] D.E. Crowley, R.S. Dungan, Metals: microbial processes affecting metals, in:
Encyclopedia of Environmental Microbiology, Wiley and Sons, Inc., New York,
2002, pp. 1878–1893.
[224] D.R. Lovley, Bioremediation of organic and metal contaminants with dissim-
ilatory metal reduction, J. Ind. Microbiol. 14 (1995) 85–93.
[225] M.N. Chandraprabha, K.A. Natarajan, Mechanism of arsenic tolerance and
bioremoval of arsenic by Acidithiobacillus ferrooxidans, J. Biochem. Technol.
3 (2011) 257–265.
[226] H. Kilty, D. Moran, J. Roussy, J.M. Tobin, C. Drakides, J.R. Degorce-Dumas,
Bioprecipitation of As and Fe ions, in: V.S.T. Ciminelli, O. Garcia (Eds.), Bio-
hydrometallurgy: Fundamentals, Technology and Sustainable Development,
Elsevier, Amsterdam, The Netherlands, 2001, pp. 365–371.
[227] M.M. Bahar, M. Megharaj, R. Naidu, Arsenic bioremediation potential of a new
arsenite-oxidizing bacterium Stenotrophomonas sp. MM-7 isolated from soil,
Biodegradation 23 (2012) 803–812.
[228] D.K. Newman, E.K. Kennedy, J.D. Coates, D. Ahmann, D.J. Ellis, D.R. Lovley,
F.M.M. Morel, Dissimilatory arsenate and sulfate reduction in Desulfotomac-
ulum auripigmentum sp., Arch. Microbiol. 168 (1997) 380–388.
[229] D. Pokhrel, T. Viraraghavan, Arsenic removal from an aqueous solution by a
modified fungal biomass, Water Res. 40 (2006) 549–552.
[230] A. Adeniji, Bioremediation of Arsenic, Chromium, Lead, and Mercury, National
Network of Environmental Management Studies Fellow for U.S. Environmen-
tal Protection Agency, Washington, DC, 2004.
[231] J. Bender, R.F. Lee, P. Phillips, A review of the uptake and transformation of
metals and metalloids by microbial mats and their use in bioremediation, J.
Ind. Microbiol. 14 (1995) 113–118.
[232] A. Chlopecka, D. Adriano, Influence of zeolite, apatite and Fe-oxide on Cd and
Pb uptake by crops, Sci. Total Environ. 207 (1997) 195–206.
[233] M.S. Pearson, K. Maenpaa, G.M. Pierzynski, M.J. Lydy, Effects of soil amend-
ment on the bioavailbility of lead, zink and cadmium to earthworms, J.
Environ. Qual. 29 (2000) 1611–1617.
[234] J. Wang, F.J. Zhao, A.A. Meharg, A. Raab, J. Feildmann, S.P. McGrath, Mech-
anisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics,
interactions with phosphate and arsenic speciation, Plant Physiol. 130 (2002)
1552–1561.
[235] T.L. Creger, F.J. Peryea, Phosphate fertilizer enhances arsenic uptake by apricot
liners grown in lead-arsenate-enriched soil, HortScience 29 (1994) 88–92.
[236] X. Cao, L.Q. Ma, M. Chen, S.P. Singh, W.G. Harris, Phosphate-induced metal
immobilization in a contaminated site, Environ. Pollut. 122 (2003) 19–28.
[237] N. Basta, S. McGowen, Evaluation of chemical immobilization treatments for
reducing heavy metal transport in a smelter-contaminated soil, Environ. Pol-
lut. 127 (2004) 73–82.
[238] M.E. Hodson, É. Valsami-Jones, J.D. Cotter-Howells, Bonemeal additions as a
remediation treatment for metal contaminated soil, Environ. Sci. Technol. 34
(2000) 3501–3507.
[239] S. Chen, M. Xu, Y. Ma, J. Yang, Evaluation of different phosphate amendments
on availability of metals in contaminated soil, Ecotoxicol. Environ. Saf. 67
(2007) 278–285.
[240] R. Liu, D. Zhao, In situ immobilization of Cu (II) in soils using a
new class of iron phosphate nanoparticles, Chemosphere 68 (2007)
1867–1876.
[241] N.S. Bolan, D.C. Adriano, P. Mani, A. Duraisamy, S. Arulmozhiselvan, Immobi-
lization and phytoavailability of cadmium in variable charge soils: II. Effect of
lime addition, Plant Soil 250 (2003) 187–198.
[242] Y.M. Li, R.L. Chaney, A.A. Schneiter, B.L. Johnson, Effect of limestone appli-
cations on cadmium content of sunflower (Helianthus annuus L.) leaves and
kernels, Plant Soil 180 (1996) 297–302.
[243] E. Lehoczky, P. Marth, I. Szabados, A. Szomolanyi, The cadmium uptake by
lettuce on contaminated soil as influenced by liming, Commun. Soil Sci. Plant
Anal. 31 (2000) 2433–2438.
[244] D.H. Han, J.H. Lee, Effect of liming on uptake of lead and cadmium by Raphanus
sativa, Arch. Environ. Contam. Toxicol. 31 (1996) 488–493.
[245] W.R. Chaney, R.C. Strickland, R.J. Lamoreaux, Phytotoxicity of cadmium inhib-
ited by lime, Plant Soil 47 (1977) 275–278.
[246] S. Brallier, R.B. Harrison, C.L. Henry, X. Dongsen, Liming effects on availability
of Cd, Cu, Ni and Zn in a soil amended with sewage sludge 16 years previously,
Water Air Soil Pollut. 86 (1996) 195–206.
[247] G. Garau, P. Castaldi, L. Santona, P. Deiana, P. Melis, Influence of red mud,
zeolite and lime on heavy metal immobilization, culturable heterotrophic
microbial populations and enzyme activities in a contaminated soil, Geo-
derma 142 (2007) 47–57.
[248] P. Castaldi, L. Santona, P. Melis, Heavy metal immobilization by chemical
amendments in a polluted soil and influence on white lupin growth, Chemo-
sphere 60 (2005) 365–371.
[249] C. Gray, S. Dunham, P. Dennis, F. Zhao, S. McGrath, Field evaluation of in situ
remediation of a heavy metal contaminated soil using lime and red-mud,
Environ. Pollut. 142 (2006) 530–539.
[250] A. Ruttens, K. Adriaensen, E. Meers, A. De Vocht, W. Geebelen, R. Carleer, M.
Mench, J. Vangronsveld, Long-term sustainability of metal immobilization by
soil amendments: cyclonic ashes versus lime addition, Environ. Pollut. 158
(2010) 1428–1434.
[251] D.H. Moon, D. Dermatas, N. Menounou, Arsenic immobilization by
calcium–arsenic precipitates in lime treated soils, Sci. Total Environ. 330
(2004) 171–185.
[252] N.S. Bolan, D.C. Adriano, A. Duraisamy, P. Mani, Immobilization and phy-
toavailability of cadmium in variable charge soils. III. Effect of biosolid
compost addition, Plant Soil 256 (2003) 231–241.
[253] N.S. Bolan, D.C. Adriano, S. Mani, A.R. Khan, Adsorption, complexation and
phytoavailability of copper as influenced by organic manure, Environ. Toxicol.
Chem. 22 (2003) 450–456.
[254] G. Merrington, C. Madden, Changes in the cadmium and zinc phytoavailability
in agricultural soil after amendment with papermill sludge and biosolids,
Commun. Soil Sci. Plant Anal. 31 (2000) 759–776.
[255] S.L. Brown, R.L. Chaney, J.S. Angle, J.A. Ryan, The phytoavailability of cadmium
to lettuces in long-term biosolids-amended soil, J. Environ. Qual. 27 (1998)
1071–1078.
[256] L.M. Shuman, S. Dudka, K. Das, Zinc forms and plant availability in a compost
amended soil, Water Air Soil Pollut. 128 (2000) 1–11.
[257] K. Weggler-Beaton, M.J. McLaughlin, R.D. Graham, Salinity increases cadmium
uptake by wheat and Swiss chard from soil amended with biosolids, Aust. J.
Soil Res. 38 (2000) 37–45.
[258] M.A. Kashem, B.R. Singh, Metal availability in contaminated soil: II. Uptake of
Cd, Ni and Zn in rice plants grown under flooded culture with organic matter
addition, Nutr. Cycl. Agroecosyst. 61 (2001) 257–266.
[259] N.S. Bolan, D.C. Adriano, R. Natesan, B.J. Koo, Effects of organic amendments
on the reduction and phytoavailability of chromate in mineral soil, J. Environ.
Qual. 32 (2003) 120–128.
[260] L. Liu, H. Chen, P. Cai, W. Liang, Q. Huang, Immobilization and phytotoxicity
of cd in contaminated soil amended with chicken manure compost, J. Hazard.
Mater. 163 (2009) 563–567.
[261] A. Ruttens, J. Colpaert, M. Mench, J. Boisson, R. Carleer, J. Vangronsveld, Phy-
tostabilization of a metal contaminated sandy soil. II. Influence of compost
and/or inorganic metal immobilizing soil amendments on metal leaching,
Environ. Pollut. 144 (2006) 533–539.
[262] J. Kumpiene, S. Ore, A. Lagerkvist, C. Maurice, Stabilization of Pb and Cu
contaminated soil using coal fly ash and peat, Environ. Pollut. 145 (2007)
365–373.
[263] Y.S. Ok, S.C. Kim, D.K. Kim, J.G. Skousen, J.S. Lee, Y.W. Cheong, S.J. Kim,
J.E. Yang, Ameliorants to immobilize Cd in rice paddy soils contaminated
by abandoned metal mines in Korea, Environ. Geochem. Health 33 (2011)
23–30.
[264] P.S. DeVolder, S.L. Brown, D. Hesterberg, K. Pandya, Metal bioavailability and
speciation in a wetland tailings repository amended with biosolids compost,
wood ash, and sulphate, J. Environ. Qual. 32 (2003) 851–864.
[265] J.H. Park, G.K. Choppala, N.S. Bolan, J.W. Chung, T. Chuasavathi, Biochar
reduces the bioavailability and phytotoxicity of heavy metals, Plant Soil 348
(2011) 439–451.
[266] M. Ahmad, S.S. Lee, J.E. Yang, H.M. Ro, Y.H. Lee, Y.S. Ok, Effects of soil dilution
and amendments (mussel shell cow bone, and biochar) on Pb availability
and phytotoxicity in military shooting range soil, Ecotoxicol. Environ. Saf. 79
(2012) 225–231.
[267] M. Mench, J. Vangronsveld, V. Didier, H. Clijsters, Evaluation of metal mobility,
plant availability and immobilization by chemical agents in a limed-silty soil,
Environ. Pollut. 86 (1994) 279–286.
 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
[268] G.M. Hettiarachchi, G.M. Pierzynski, M.D. Ransom, In situ stabilization of soil
lead using phosphorus and manganese oxide, Environ. Sci. Technol. 34 (2000)
4614–4619.
[269] M. Contin, C. Mondini, L. Leita, M.D. Nobili, Enhanced soil toxic metal fixation
in iron (hydr) oxides by redox cycles, Geoderma 140 (2007) 164–175.
[270] S. Cheng, Z. Hseu, In-situ immobilization of cadmium and lead by different
amendments in two contaminated soils, Water Air Soil Pollut. 140 (2002)
73–84.
[271] W. Hartley, N.W. Lepp, Remediation of arsenic contaminated soils by iron-
oxide application evaluated in terms of plant productivity, arsenic and
phytotoxic metal uptake, Sci. Total Environ. 390 (2008) 35–44.
[272] A. Chlopecka, D.C. Adriano, Mimicked in-situ stabilization of metals in a
cropped soil: bioavailability and chemical form of zinc, Environ. Sci. Technol.
30 (1996) 3294–3303.
[273] M. Chrysochoou, D. Dermatas, D.G. Grubb, Phosphate application to firing
range soils for Pb immobilization: the unclear role of phosphate, J. Hazard.
Mater. 144 (2007) 1–14.
[274] Q.Y. Ma, T.J. Logan, S.J. Traina, Lead immobilization from aqueous solutions
and contaminated soils using phosphate rocks, Environ. Sci. Technol. 29
(1995) 1118–1126.
[275] P. Ndiba, L. Axe, T. Boonfueng, Heavy metal immobilization through phos-
phate and thermal treatment of dredged sediments, Environ. Sci. Technol. 42
(2008) 920–926.
[276] A.G.B. Williams, K.G. Scheckel, G. McDermott, D. Gratson, D. Neptune, J.A.
Ryan, Speciation and bioavailability of zinc in amended sediments, Chem.
Spec. Bioavail. 23 (2011) 163–174.
[277] K. Kim, S. Lee, J. Ammons, Immobilization of radioactive strontium in con-
taminated soils by phosphate treatment, MRS Proc. 212 (1990) 633.
[278] G.S.R. Krishnamurti, P.M. Huang, K.C.J. Van Rees, Studies on soil rhizo-
sphere: speciation and availability of cadmium, Chem. Spec. Bioavail. 8 (1996)
23–28.
[279] G.A. O’Connor, C. O’Connor, G.R. Cline, Sorption of cadmium by calcare-
ous soils: influence of solution composition, Soil Sci. Soc. Am. J. 48 (1984)
1244–1247.
[280] J.H. Park, N.S. Bolan, M. Megharaj, R. Naidu, Comparative value of phosphate
sources on the immobilization of lead, and leaching of lead and phosphorus
in lead contaminated soils, Sci. Total Environ. 409 (2011) 853–860.
[281] J.H. Park, N.S. Bolan, J.W. Chung, R. Naidu, Environmental monitoring of the
role of phosphate compounds in enhancing immobilization and reducing
bioavailability of lead in contaminated soils, J. Environ. Monit. 13 (2011)
2234–2242.
[282] Y.S. Ok, J.E. Lim, D.H. Moon, Stabilization of Pb and Cd contaminated soils
and soil quality improvements using waste oyster shells, Environ. Geochem.
Health 33 (2011) 83–91.
[283] Y.S. Ok, S.S. Lee, W.T. Jeon, S.E. Oh, A.R.A. Usman, D.H. Moon, Application of
eggshell waste for the immobilization of cadmium and lead in a contaminated
soil, Environ. Geochem. Health 33 (2011) 31–39.
[284] M. Fang, J. Wong, Effects of lime amendment on availability of heavy metals
and maturation in sewage sludge composting, Environ. Pollut. 106 (1999)
83–89.
[285] J. Singh, A.S. Kalamdhad, Effects of lime on bioavailability and leachability of
heavy metals during agitated pile composting of water hyacinth, Bioresour.
Technol. 138 (2013) 148–155.
[286] M. Pantsar-Kallio, S.P. Reinikainen, M. Oksanen, Interactions of soil compo-
nents and their effects on speciation of chromium in soils, Anal. Chim. Acta
439 (2001) 9–17.
[287] C. Bourotte, R. Bertolo, M. Almodovar, R. Hirata, Natural occurrence of hexava-
lent chromium in a sedimentary aquifer in Urânia, State of São Paulo, Brazil,
An. Acad. Bras. Cienc. 81 (2009) 227–242.
[288] U.N. Rai, S. Pandey, S. Sinha, A. Singh, R. Saxena, D.K. Gupta, Revegetating fly
ash landfills with Prosopis juliflora L.: impact of different amendments and
Rhizobium inoculation, Environ. Int. 30 (2004) 293–300.
[289] A. Zorpas, T. Constantinides, A. Vlyssides, I. Haralambous, M. Loizidou, Heavy
metal uptake by natural zeolite and metals partitioning in sewage sludge
compost, Bioresour. Technol. 72 (2000) 113–119.
[290] S. Brown, R.L. Chaney, J.G. Hallfrisch, Q. Xue, Effect of biosolids processing on
lead bioavailability in an urban soil, J. Environ. Qual. 32 (2003) 100–108.
[291] Y.M. Li, R.L. Chaney, G. Siebielec, B.A. Kerschner, Response of four turfgrass cul-
tivars to limestone and biosolids-compost amendment of a zinc and cadmium
contaminated soil at Palmerton, Pennsylvania, J. Environ. Qual. 29 (2000)
1440–1447.
[292] I.V. Perminova, K. Hatfield, Remediation chemistry of humic substances:
theory and implications for technology, in: I.V. Perminova, N. Hertkorn, K. Hat-
field (Eds.), Use of Humic Substances to Remediate Polluted Environments:
From Theory to Practice, NATO Science Series: IV. Earth and Environmental
Sciences, vol. 52, Springer, Dordrecht, 2005, pp. 3–36.
[293] J. Kumpiene, Trace element immobilization in soil using amendments, in: P.
Hooda (Ed.), Trace Elements in Soils, John Wiley and Sons Ltd., Wiltshire, UK,
2010, pp. 353–380.
[294] M. Komárek, A. Vaněk, V. Ettler, Chemical stabilization of metals and arsenic
in contaminated soils using oxides – a review, Environ. Pollut. 172 (2013)
9–22.
[295] A. Knox, J. Seaman, M. Mench, J. Vangronsveld, Remediation of metal-and
radionuclides-contaminated soils by in situ stabilization techniques, in:
I.K. Iskandar (Ed.), Environmental Restoration of Metals-Contaminated Soil,
Lewis Publishers, Boca Raton, FL, 2001, pp. 21–61.
165
[296] W. Hartley, R. Edwards, N.W. Lepp, Arsenic and heavy metal mobility in
iron oxide-amended contaminated soils as evaluated by short-and long-term
leaching tests, Environ. Pollut. 131 (2004) 495–504.
[297] C.A. Impellitteri, K.G. Scheckel, The distribution, solid-phase speciation, and
desorption/dissolution of As in waste iron-based drinking water treatment
residuals, Chemosphere 64 (2006) 875–880.
[298] X.H. Feng, L.M. Zhai, W.F. Tan, F. Liu, J.Z. He, Adsorption and redox reactions of
heavy metals on synthesized Mn oxide minerals, Environ. Pollut. 147 (2007)
366–373.
[299] N. Miyata, Y. Tani, M. Sakata, K. Iwahori, Microbial manganese oxide formation
and interaction with toxic metal ions, J. Biosci. Bioeng. 104 (2007) 1–8.
[300] M. Hua, S. Zhang, B. Pan, W. Zhang, L. Lv, Q. Zhang, Heavy metal removal from
water/wastewater by nanosized metal oxides: a review, J. Hazard. Mater. 211
(2012) 317–331.
[301] A. Rahmani, H.Z. Mousavi, M. Fazli, Effect of nanostructure alumina on adsorp-
tion of heavy metals, Desalination 253 (2010) 94–100.
[302] S. Joseph, M. Camps-Arbestain, Y. Lin, P. Munroe, C. Chia, J. Hook, B. Singh, An
investigation into the reactions of biochar in soil, Soil Res. 48 (2010) 501–515.
[303] R. Kookana, A. Sarmah, L. Van Zwieten, E. Krull, B. Singh, Biochar application to
soil: agronomic and environmental benefits and unintended consequences,
Adv. Agron. 112 (2011) 103–143.
[304] W. Hartley, N.M. Dickinson, R. Clemente, C. French, T.G. Piearce, S. Sparke,
N.W. Lepp, Arsenic stability and mobilization in soil at an amenity grass-
land overlying chemical waste (St. Helens, UK), Environ. Pollut. 157 (2009)
847–856.
[305] M. Uchimiya, D.I. Bannon, L.H. Wartelle, I.M. Lima, K.T. Klasson, Lead reten-
tion by broiler litter biochars in small arms range soil: impact of pyrolysis
temperature, J. Agric. Food Chem. 60 (2012) 5035–5044.
[306] M. Uchimiya, K.T. Klasson, L.H. Wartelle, I.M. Lima, Influence of soil properties
on heavy metal sequestration by biochar amendment: 1. Copper sorption
isotherms and the release of cations, Chemosphere 82 (2011) 1431–1437.
[307] X. Cao, L. Ma, Y. Liang, B. Gao, W. Harris, Simultaneous immobilization of lead
and atrazine in contaminated soils using dairy-manure biochar, Environ. Sci.
Technol. 45 (2011) 4884–4889.
[308] M. Uchimiya, S. Chang, K.T. Klasson, Screening biochars for heavy metal reten-
tion in soil: role of oxygen functional groups, J. Hazard. Mater. 190 (2011)
432–441.
[309] H.P. Boehm, Some aspects of the surface chemistry of carbon blacks and other
carbons, Carbon 32 (1994) 759–769.
[310] E.D. Goldberg, Black Carbon in the Environment: Properties and Distribution,
John Wiley & Sons Inc., New York, 1985.
[311] R. Zimmerman, Abiotic and microbial oxidation of laboratory-produced black
carbon (Biochar), Environ. Sci. Technol. 44 (2010) 1295–1301.
[312] J. Vangronsveld, R. Herzig, N. Weyens, J. Boulet, K. Adriaensen, A. Ruttens, T.
Thewys, A. Vassilev, E. Meers, E. Nehnevajova, D. Van der Lelie, M. Mench,
Phytoremediation of contaminated soils and groundwater: lessons from the
field, Environ. Sci. Pollut. Res. 16 (2009) 765–794.
[313] G. Dermont, M. Bergeron, G. Mercier, M. Richer-Lafleche, Metal contaminated
soils: remediation practices and treatment technologies, Pract. Period. Haz-
ard. Toxic Radioact. Waste Manage. 12 (2008) 188–209.
[314] H.A. Elliott, L.M. Herzig, Oxalate extraction of Pb and Zn from polluted soils:
solubility limitations, J. Soil Contam. 8 (1999) 105–116.
[315] T. Makino, K. Sugahara, Y. Sakurai, H. Takano, T. Kamiya, K. Sasaki, T. Itou, N.
Sekiya, Remediation of cadmium contamination in paddy soils by washing
with chemicals: selection of washing chemicals, Environ. Pollut. 144 (2006)
2–10.
[316] T. Makino, T. Kamiya, H. Takano, T. Itou, N. Sekiya, K. Sasaki, Y. Sugahara,
Y. Maejima, Remediation of cadmium-contaminated paddy soils by washing
with calcium chloride: verification of on-site washing, Environ. Pollut. 147
(2007) 112–119.
[317] R.J. Abumaizar, E.H. Smith, Heavy metal contaminants removal by soil wash-
ing, J. Hazard. Mater. 70 (1999) 71–86.
[318] Q.R. Zeng, S. Sauve, H.E. Allen, W.H. Hendershot, Recycling EDTA solu-
tions used to remediate metal-polluted soils, Environ. Pollut. 133 (2005)
225–231.
[319] S. Tandy, K. Bossart, R. Mueller, J. Ritschel, L. Hauser, R. Schulin, B. Nowack,
Extraction of heavy metals from soils using biodegradable chelating agents,
Environ. Sci. Technol. 38 (2004) 937–944.
[320] S.H. Chang, K.S. Wang, C.Y. Kuo, C.Y. Chang, C.T. Chou, Remediation of metal-
contaminated soil by an integrated soil washing-electrolysis process, Soil
Sediment Contam. 14 (2005) 559–569.
[321] K.J. Hong, S. Tokunaga, T. Kajiuchi, Evaluation of remediation process with
plant-derived biosurfactant for recovery of heavy metals from contaminated
soils, Chemosphere 49 (2002) 379–387.
[322] C.N. Mulligan, R.N. Yong, B.F. Gibbs, Removal of heavy metals from contam-
inated soil and sediments using the biosurfactant surfactin, J. Soil Contam. 8
(1999) 231–254.
[323] T. Makino, H. Takano, T. Kamiya, T. Itou, N. Sekiya, M. Inahara, Y. Sakurai,
Restoration of cadmium-contaminated paddy soils by washing with ferric
chloride: Cd extraction mechanism and bench-scale verification, Chemo-
sphere 70 (2008) 1035–1043.
[324] J.S. Dube, R. Galvez-Cloutier, Applications of data on the mobility of heavy
metals in contaminated soil to the definition of site-specific remediation
criteria, J. Environ. Eng. Sci. 4 (2005) 399–411.
[325] J. Kumpiene, G. Guerri, L. Landi, G. Pietramellara, P. Nannipieri, G. Renella,
Microbial biomass, respiration and enzyme activities after in situ aided
166 N. Bolan et al. / Journal of Hazardous Materials 266 (2014) 141–166
phytostabilization of a Pb- and Cu-contaminated soil, Ecol. Environ. Safe. 72
(2009) 115–119.
[326] W. Friesl-Hanl, K. Platzer, O. Horak, M.H. Gerzabek, Immobilising of Cd, Pb,
and Zn contaminated arable soils close to a former Pb/Zn smelter: a field study
in Austria over 5 years, Environ. Geochem. Health 31 (2009) 581–594.
[327] L.A. Oste, J. Dolfing, W.C. Ma, T.M. Lexmond, Effect of beringite on cadmium
and zinc uptake by plants and earthworms: more than a liming effect? Envi-
ron. Toxicol. Chem. 20 (2001) 1339–1345.
[328] C.C. Ainsworth, J.P. Pilon, P.L. Gassman, W.G. Van der Sluys, Cobalt, cadmium
and lead sorption to hydrous iron oxide: residence time effect, Soil Sci. Soc.
Am. J. 58 (1994) 1615–1632.
[329] M. Mench, J. Vangronsveld, C. Beckx, A. Ruttens, Progress in assisted natural
remediation of an arsenic contaminated agricultural soil, Environ. Pollut. 144
(2006) 51–61.
[330] G. Renella, L. Landi, J. Ascher, M.T. Ceccherini, G. Pietramellara, M. Mench, P.
Nannipieri, Long-term effects of aided phytostabilisation of trace elements on
microbial biomass and activity enzyme activities, and composition of micro-
bial community in the Jales contaminated mine spoils, Environ. Pollut. 152
(2008) 702–712.
[331] A. Ruttens, M. Mench, J.V. Colpaert, J. Boisson, R. Carleer, J. Vangronsveld,
Phytostabilization of a metal contaminated sandy soil. I: Influence of compost
and/or inorganic metal immobilizing soil amendments on phytotoxicity and
plant availability of metals, Environ. Pollut. 144 (2006) 524–532.
[332] J. Kumpiene, P. Desogus, S. Schulenburg, M. Arenella, G. Renella, E. Brän-
nvall, A. Lagerkvist, L. Andreas, R. Sjöblom, Utilisation of chemically stabilized
arsenic-contaminated soil in a landfill cover, Environ. Sci. Pollut. Res. (2013),
http://dx.doi.org/10.1007/s11356-013-1818-3.
[333] J.A. Ryan, K.G. Scheckel, W.R. Berti, S.L. Brown, S.W. Casteel, R.L. Chaney, J.
Hallfrisch, M. Doolan, P. Grevatt, M. Maddaloni, D. Mosby, Reducing children’s
risk from lead in soil, Environ. Sci. Technol. 38 (2004) 18A–24A.
[334] K.G. Scheckel, J.A. Ryan, Spectroscopic speciation and quantification of lead
in phosphate-amended soils, J. Environ. Qual. 33 (2004) 1288–1295.
[335] K.G. Scheckel, J.A. Ryan, D. Allen, N.V. Lescano, Determining speciation of Pb in
phosphate-amended soils: method limitations, Sci. Total Environ. 350 (2005)
261–272.
[336] M. Maddaloni, N. Lolacono, W. Manton, C. Blum, J. Drexler, J. Graziano,
Bioavailability of soil borne lead in adults, by stable isotope dilution, Environ.
Health Perspect. 106 (1998) 1589–1594.
[337] B. Sun, F.J. Zhao, E. Lombi, S.P. McGrath, Leaching of heavy metals from con-
taminated soils using EDTA, Environ. Pollut. 113 (2001) 111–120.
[338] W.W. Wenzel, R. Unterbrunner, P. Sommer, P. Sacco, Chelate-assisted phy-
toextraction using canola (Brassica napus L.) in outdoors pot and lysimeter
experiments, Plant Soil 249 (2003) 83–96.
[339] L.H. Wu, Y.M. Luo, X.R. Xing, P. Christie, EDTA-enhanced phytoremediation of
heavy metal contaminated soil with Indian mustard and associated potential
leaching risk, Agric. Ecosyst. Environ. 102 (2004) 307–318.
[340] H. Grčman, D. Velikonja-Bolta, D. Vodnik, B. Kos, D. Leštan, EDTA enhanced
heavy metal phytoextraction: metal accumulation, leaching, and toxicity,
Plant Soil 235 (2001) 105–114.
[341] M. Komárek, A. Vaněk, L. Mrnka, R. Sudová, J. Száková, V. Tejnecký, V. Chrastný,
Potential and drawbacks of EDDS-enhanced phytoextraction of copper from
contaminated soils, Environ. Pollut. 158 (2010) 2428–2438.
[342] H. Grčman, D. Vodnik, S. Velikonja-Bolta, D. Lestan, Ethylenediaminedis-
succinate as a new chelate for environmentally safe enhanced lead
phytoextraction, J. Environ. Qual. 32 (2003) 500–506.
[343] I.M.C. Lo, D.C.W. Tsang, T.C.M. Yip, F. Wang, W. Zhang, Significance of metal
exchange in EDDS-flushing column experiments, Chemosphere 83 (2011)
7–13.
[344] C.L. Luo, Z.G. Shen, X.D. Li, Enhanced phytoextraction of Cu, Pb, Zn and Cd with
EDTA and EDDS, Chemosphere 59 (2005) 1–11.
[345] E. Meers, A. Ruttens, M.J. Hopgood, D. Samson, F.M.G. Tack, Comparison of
EDTA and EDDS as potential soil amendments for enhanced phytoextraction
of heavy metals, Chemosphere 58 (2005) 1011–1022.
[346] E. Meers, F.M.G. Tack, M.G. Verloo, Degradability of ethylenediaminedisuc-
cinic acid (EDDS) in metal contaminated soils: implications for its use soil
remediation, Chemosphere 70 (2008) 358–363.
[347] P.C. Vandevivere, H. Saveyn, W. Verstraete, T.C. Feijtel, D.R. Schowanek,
Biodegradation of metal-[S, S]–EDDS complexes, Environ. Sci. Technol. 35
(2001) 1765–1770.
[348] T. Thayalakumaran, B.H. Robinson, I. Vogeler, D.R. Scotter, B.E. Clothier, H.J.
Percival, Plant uptake and leaching of copper during EDTA-enhanced phytore-
mediation of repacked and undisturbed soil, Plant Soil 254 (2003) 415–423.
[349] I. Vogeler, T. Thayalakumaran, Transport and reactions of EDTA in soils: exper-
iments and modeling, in: B. Nowack, J. VanBriesen (Eds.), Biogeochemistry of
Chelating Agents, ACS Symposium Series, vol. 910, 2005, pp. 316–335.
[350] Z.G. Shen, X.D. Li, C.C. Wang, H.M. Chen, H. Chua, Lead phytoextraction from
contaminated soil with high-biomass plant species, J. Environ. Qual. 31 (2002)
1893–1900.
[351] B.E. Clothier, S.R. Green, Roots: the big movers of water and chemical in soil,
Soil Sci. 162 (1997) 534–543.
[352] G.A. Brown, H.A. Elliott, Influence of electrolytes on EDTA extraction of Pb
from polluted soil, Water Air Soil Pollut. 62 (1992) 157–165.
[353] I.M.C. Lo, X.Y. Yang, EDTA extraction of heavy metals from different soil frac-
tions and synthetic soils, Water Air Soil Pollut. 109 (1999) 219–236.
[354] Z. Hu, K. Chandran, D. Grasso, B.F. Smets, Nitrification inhibition by
ethylenediamine-based chelating agents, Environ. Eng. Sci. 20 (2003)
219–228.
[355] Y.X. Chen, Y.P. Wang, W.X. Wu, Q. Lin, S.G. Xue, Impacts of chelate-assisted
phytoremediation on microbial community composition in the rhizosphere
of a copper accumulator and non-accumulator, Sci. Total Environ. 356 (2006)
247–255.
[356] C.K. Schmidt, M. Fleig, F. Sacher, H.J. Brauch, Occurrence of aminopolycar-
boxylates in the aquatic environment of Germany, Environ. Pollut. 131 (2004)
107–124.
[357] F.J. Peryea, Phosphorus starter fertilizer temporarily enhances soil arsenic
uptake by apple trees grown under field conditions, Hort. Sci. 33 (1998)
826–829.
[358] F.J. Peryea, R. Kammereck, Phosphate enriched movement of arsenic out of
lead arsenate contaminated topsoil and through uncontaminated subsoil,
Water Air Soil Pollut. 93 (1997) 243–254.
[359] E.E. Codling, T.H. Dao, Short-term effect of lime, phosphorus, and iron amend-
ments on water-extractable lead and arsenic in orchard soils, Commun. Soil
Sci. Plant Anal. 38 (2007) 903–919.
[360] N. Caille, S. Swanwick, F.J. Zhao, S.P. McGrath, Arsenic hyperaccumulation by
Pteris vittata from arsenic contaminated soils and the effect of liming and
phosphate fertilization, Environ. Pollut. 132 (2004) 113–120.
[361] E. Kurek, M. Majewska, In vitro remobilization of Cd immobilized by fungal
biomass, Geoderma (2004) 235–246.
[362] A. Bourg, J.G. Loch, Mobilization of heavy metals as affected by pH and redox
conditions, in: Biogeodynamics of Pollutants in Soils and Sediments, Springer,
1995, pp. 87–102.
[363] S. Tandy, J.R. Healey, M.A. Nason, J.C. Williamson, D.L. Jones, Remediation of
metal polluted mine soil with compost: co-composting versus incorporation,
Environ. Pollut. 157 (2009) 690–697.
[364] R. Clemente, Á. Escolar, M.P. Bernal, Heavy metals fractionation and organic
matter mineralisation in contaminated calcareous soil amended with organic
materials, Bioresour. Technol. 97 (2006) 1894–1901.
[365] M.M. Urrutia, T.J. Beveridge, Remobilization of heavy metals retained as oxy-
hydroxides or silicates by Bacillus subtilis cells, Appl. Environ. Microbiol. 59
(1993) 4323–4329.
[366] L.R. Baker, P.M. White, G.M. Pierzynski, Changes in microbial properties after
manure, lime, and bentonite application to a heavy metal-contaminated mine
waste, Appl. Soil Ecol. 48 (2011) 1–10.
[367] J. Kumpiene, D. Ragnvaldsson, L. Lövgren, S. Tesfalidet, B. Gustavsson, A.
Lättström, P. Leffler, C. Maurice, Impact of water saturation level on arsenic
and metal mobility in the Fe-amended soil, Chemosphere 74 (2009) 206–215.
[368] M. Manecki, P.A. Maurice, Siderophore promoted dissolution of pyromor-
phite, Soil Sci. 173 (2008) 821–830.
[369] K.G. Scheckel, J.A. Ryan, Effects of aging and pH on dissolution kinetics and
stability of chloropyromorphite, Environ. Sci. Technol. 36 (2002) 2198–2204.
[370] N. Basta, R. Gradwohl, K. Snethen, J. Schroder, Chemical immobilization of
lead, zinc, and cadmium in smelter-contaminated soils using biosolids and
rock phosphate, J. Environ. Qual. 30 (2001) 1222–1230.
[371] Y. Fang, X. Cao, L. Zhao, Effects of phosphorus amendments and plant growth
on the mobility of Pb, Cu, and Zn in a multi-metal-contaminated soil, Environ.
Sci. Pollut. Res. 19 (2012) 1659–1667.
[372] F. Bartoli, D. Coinchelin, C. Robin, G. Echevarria, Impact of active transport and
transpiration on nickel and cadmium accumulation in the leaves of the Ni-
hyperaccumulator Leptoplax emarginata: a biophysical approach, Plant Soil
350 (2012) 99–115.
[373] N. Garg, N. Aggarwal, Effect of mycorrhizal inoculations on heavy metal
uptake and stress alleviation of Cajanus cajun (L.) Millsp. genotypes grown in
cadmium and lead contaminated soils, Plant Growth Regul. 66 (2012) 9–26.
[374] F. Degryse, A. Shahbazi, L. Verheyen, E. Smolders, Diffusion limitations in root
uptake of cadmium and zinc, but not nickel, and resulting bias in the Michaelis
constant, Plant Physiol. 160 (2012) 1097–1109.
[375] F. Madrid, M.S. Liphadzi, M.B. Kirkham, EDTA-assisted phytostabilization by
barley roots contaminated with heavy metals, in: R. Naidu (Ed.), Chemical
Bioavailability in Terrestrial Environments, Developments in Soil Science, vol.
32, Elsevier, Amsterdam, 2008, pp. 697–718.