Geoderma 122 (2004) 143 – 149

www.elsevier.com/locate/geoderma

Soil–plant transfer of trace elements—an environmental issue

Alina Kabata-Pendias
Institute of Soil Science and Cultivation of Plants, 24-100 Pulawy, Poland

Available online 27 February 2004

Abstract

The transfer of trace elements within the soil – plant chain is a part of the biochemical cycling of chemical elements—it is an
element flow from nonliving to the living compartments of the biosphere. Several factors control the processes of mobility and
availability of elements; in general, they are of geochemical, climatic, biological, as well as of anthropogenic origin.
The soil is a heterogeneous mixture of different organisms and mineral, organic and organo-mineral substances present in
three phases: solid, liquid, gaseous. Thus, trace metals occur in different species according to whether they are external or
internal bound to various soil components or in the liquid phase. The solubility of elements, thus, their concentration in the soil
solution depend upon the solubility equilibrium. However, the equilibrium constant is constant only under specific conditions.
Therefore, the solution equilibrium for soil phases is not easy to predict. So, in order to assess the speciation or binding forms of
trace elements in soil material, different analytical procedures have been developed, including successive extraction methods
applied broadly for the speciation of trace metals.
Criteria for environmental protection related to the trace element status in soils should consider all the major variables that
govern their behavior, and in particular those that control their mobility and soil – plant transfer.
D 2004 Elsevier B.V. All rights reserved.

Keywords: Trace elements in soil; Cycling; Mobility; Phytoavailability

1. Introduction environment and human health of a given trace element

The soil –plant transfer of trace elements is a part of
chemical element cycling in the nature. It is a very
complex process governed by several factors, both
natural and affected by man. Several factors control
the processes of mobility and availability of elements;
in general, they are of geochemical, climatic and
biological origin. Thus, the prediction of trace element
uptake by plants from a given growth media should be
based on several biotic and abiotic parameters that
control their behavior in soil. The risk to both the
E-mail address: akp@iung.pulawy.pl (A. Kabata-Pendias).
is a function of its mobility and phytoavailability.
Therefore, the behavioral properties of these elements
in soils are a current issue in environmental studies.
2. Trace elements in soil
Soil is the main source of trace elements for plants
both as micronutrients and pollutants. Some exceptions
are in situations of heavy atmospheric deposition of
pollutants or from flooding by contaminated waters.
Soil conditions play a crucial role in trace element
behavior (Table 1). It can be generalized that in well-

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doi:10.1016/j.geoderma.2004.01.004
144 A. Kabata-Pendias / Geoderma 122 (2004) 143–149

Table 1 The cation and anion exchange capacity (CEC,

Bioavailability of trace metals under different soil conditionsa AEC) of a soil for trace elements is closely associated
Soil condition Bioavailability with the specific surface area of the soil particles. This
Redox pH Easy Moderate value varies for different clay minerals within the
Oxidizing <3 Cd, Zn, Co, Mn, Hg, V range from 25 up to above 800 m2/g (Table 3), and
Cu, Ni for SOM is has been calculated to be 560 –800 m2/g.
Oxidizing >5 Cd, Zn Mo, Se, Sr, The contribution of SOM to CEC is significant in most
Te, V
arable soils and varies from 25% to 90%, depending on
Oxidizing >5 Non Cd, Zn
Fe-rich the soil type. A special influence of DOC (operation-
Reducing >5 Se, Mo Cd, Zn, Cu, ally defined as the dissolved organic carbon which
Mn, Pb, Sr passes through a 0.45-Am filter) due to a strong metal
Reducing, >5 Non Mn, Sr binding can change the impact of SOM on the behav-
with H2S
ior of some metals (Al-Wabel et al., 2002). However,
a
After Kabata-Pendias and Pendias (2001) and Smith and hydroxides of Fe and Mn, due to their wide distribu-
Huyck (1999).
tion mainly as coatings on soil particles, as well as due
to their great sensitivity to variation in redox potential,
aerated (oxidizing) acid soils, several trace metals, play the most important role in the distribution and
especially Cd and Zn, are easily mobile and available behavior of trace elements, in particular those that
to plants, while in poorly aerated (reducing) neutral or occur in anionic form. In particular, Mn is described as
alkaline soils, metals are substantially less available. a very important metallic redox catalyst, that governs
All other metals not cited in the Table 1 are slightly less the behavior of most trace metals in soils (Bartlett,
available to plants under the described soil conditions. 1999). Extremely high concentrations (up to about 1
The origin of trace elements influences their be- AM g 1) of trace metals (e.g., Zn, V, Cr, Pb) are
havior in soils and therefore controls to some extent observed in goethite and manganese-rich soil nodules.
their bioavailability (Table 2). Lithogenic elements are All metals that are especially susceptible to redox
associated either with primary minerals, or with sec- reactions, e.g., Co, Cr, Fe, are also involved in disso-
ondary minerals (mainly clay minerals) that occur in lution/precipitation processes in a soil. These metals
the parent material. Their mobility depends firstly on can be easily either oxidized or reduced under variable
weathering processes, and secondly on the anion soil conditions and can influence the mobility and
(AEC) and cation exchange capacity (CEC) of min- bioavailability of associated trace elements (Table 1).
erals. Pedogenic trace elements are both of lithogenic The impact of soil microorganisms and enzymes
and anthropogenic origin, but their distribution and (in particular those produced by microbes in the
speciation are affected as a result of various pedogenic rhiziplane) on all redox and dissolution/precipitation
processes, among which the fixation by clay minerals processes is very crucial and can exert a high degree
and binding/complexing by soil organic matter (SOM) of control on the behavior of trace elements (Burns
play a crucial role. and Dick, 2002). Especially biological methylation of

Table 2
Influence of origin of trace elements on their behavior in soil
Origin Association Phase Forma Bioavailability
Lithogenic Bound to minerals, Solid Residual Very slight
Pedogenic CM, SOM, and OX Solid Fixed by CM, Slight
SOM, and OX
Anthropogenic SOM and PS Solid Exchangeable Moderate
and chelated
Pedogenic and Simple or complexed Aqueous Easily High
anthropogenic ions soluble
CM: clay minerals, SOM: soil organic matter, OX: oxides, PS: particle surface.
a
Operational fractions according to the sequential extraction (Tessier et al., 1979).
 A. Kabata-Pendias / Geoderma 122 (2004) 143–149 145

Table 3 The concentration of free metal ion species in the

Surface area and sorption properties of common soil mineralsa soil solution is controlled by several factors of which
Mineral Total or specific Cation exchange the most significant are thermodynamic/kinetic
surface (m2/g) capacity
parameters. Mathematical approaches to modeling
(cmol(+)/kg)
soil solution –solid phase equilibria are broadly de-
Allophane 100 – 880 5 – 350
scribed in numerous reports (Wolt, 1994; Sparks,
Kaolinite 7 – 30 3 – 22
Halloysite 10 – 45 3 – 57 1999; Suarez, 1999). However, mathematical model-
Montmorillonite 280 – 800 80 – 150 ing can only give some boundary conditions. More-
Illite 65 – 100 20 – 50 over, trends in the distribution of trace element species
Chlorite 25 – 150 10 – 40 could be indicated, especially in systems for which the
Vermiculitesb 50 – 800 10 – 200
determination of concentrations of all species of
Goethite 41 – 81
(305 – 412)c 160c interest is impossible because of sensitivity constraints
Mn oxide 32 – 300 150 – 230 or other analytical difficulties.
Muscovite 60 – 100 10 – 40 Methods used for obtaining soil solution differ
Plagioclases – 7 widely, and therefore, it is difficult to adequately access
Quartz 2–3 7
mean concentrations for trace elements in the soil
a
Data sources: Bolt (1979), Kabata-Pendias and Pendias (2001), solution. The ranges of some elements measured in
Tan (1998), Sparks (1995).
b the solution obtained by various techniques from
Dioctahedral and trioctahedral vermiculites.
c
Amorphous Fe oxides. uncontaminated soils are, as follows (in Ag/l): B 12 –
800, Cd 0.01 –5, Co 0.3– 29, Cr 0.4 –29, Cu 0.5 –135,
some elements, such as: As, Hg, Se, Te, Tl and Pb has Mn 25– 8000, Mo 2 –30, Ni 3 –150, Pb 0.6– 63, and Zn
a significant impact on their behavior. 1 – 750 (Kabata-Pendias and Pendias, 2001). Wolt
(1994) presented mean natural abundance of trace
elements in soil solution as follows (in Amol/l): As
3. Trace elements in soil solution 0.01, B 5, Be 0.1, Cd 0.04, Co 0.08, Cr 0.01, Cu 1, Hg
0.0005, I 0.08, Mo 0.0004, Ni 0.17, Pb 0.005, Se 0.06,
Transfer of trace elements between soil phases can Sn 0.2, and Zn 0.08.
be considered as the main processes controlling their In general, the total contents of trace elements in
behavior and bioavailability. However, the soil liquid solutions of uncontaminated mineral soils range from
phase (soil solution) is constantly and rapidly chang- 1 to 100 Ag/l, while in contaminated soils these values
ing in amount and chemical composition due to the can be much higher. In both kinds of soils, however,
contact with the highly diverse soil solid phase and by these are negligible portions of the total concentra-
the uptake of ions and water by plant roots. tions of soil metals. The transfer factor, calculated as a
The chemistry of the soil solution provides useful ratio of metals in solution of contaminated soils to
information on soil processes that are important to their contents in a solution of the control soils usually
agricultural and environmental sciences. Therefore, decrease in the following order: Cd>Ni>Zn>
data on concentrations of trace elements in a ‘‘real’’ Cu>Pb>Cr (Kabata-Pendias and Pendias, 2001).
soil solution can be useful for the prediction of their
availability, toxic effects on crops and on the bio-
logical activities in soils. The partitioning of trace 4. Speciation of trace metals
elements between the soil solid phase and the soil
solution determines their mobility and bioavailability. Speciation (in the context of soils) refers to both the
However, predicting the properties of soil solutions process and the quantification of the different defined
is difficult, and sophisticated techniques must be species, forms and phases of a trace element. The
used for the obtaining undiluted soil solution. The speciation of trace metals in soils is related to their
impact of variations in the redox potentials on the biogeochemical reactivity and to several physicochem-
properties of stored soil/sediment samples should be ical conditions of the soil. Determinations of various
also considered. fractions of these elements are broadly used especially
146 A. Kabata-Pendias / Geoderma 122 (2004) 143–149
for two purposes, to link with the potential bioavail-
ability, and to predict the mobility affecting their
transport to groundwater. A number of different selec-
tive extraction procedures show a great diversity
among reagents used for the determination of com-
monly distinguished metal species which are, in gen-
eral: (a) easily exchangeable or water soluble, (b)
specifically sorbed, e.g., by carbonates, or phosphates,
(c) organically bound, (d) occluded in Fe/Mn oxides
and hydroxides, and (e) structurally bound in minerals
(residual). However, the speciation of metals in soils is
not stable, and relatively easy transformation of their
forms in soils is observed.
Depending upon the variability in physico-chemi-
cal characteristics of metals, their affinity to soil
components governs their speciation. Rule (1999)
broadly reviewed recent literature on the phase distri-
bution of trace metals in soils and concluded that the
highest proportions of most metals are found either in
residual, or in Fe –Mn oxide fractions in both natural
and contaminated soils. A strong association with the
exchangeable fraction was observed only for Cd in a
few soils. Cd and Zn were also abundant in the
carbonate fraction in some soils. The association of
metals with organic matter also has a significant
impact on their behavior.
5. Soil – plant transfer of trace elements
The bioavailability of trace elements has been the
most crucial problem in agricultural and environmental
studies. There has been a steady increase in the number
of investigations related to both understanding the
processed involved in the uptake of an element (nutri-
ent and non-nutrient) by plants, and to finding the most
reliable methods for the prediction of availability of a
given element to plants, and in particular to crop plants.
Plants have developed during their evolution several
biochemical mechanisms that have resulted in adapta-
tion to, and tolerance of, new or chemically imbalanced
growth media. Therefore, plant responses to trace
elements in the soil and ambient air can vary and
should always be investigated for the particular soil –
plant system.
It is known that plant roots exude substances that are
involved in the uptake mechanisms. Root and rhizo-
plane exudates are variable in composition but normal-
ly consist of low molecular weight compounds. For
example, compounds released from tree (Pinus spe-
cies) roots are mainly acetic acid, oxalic acid and amino
acids (Smith, 1969). The composition of root exudates
can greatly change under any environmental stress. The
excess of trace metals in soils is a stronger stress to
plants than their deficiency and some plants can devel-
op a protective mechanism against an excess, in par-
ticular, of metals. These mechanisms, however, can
operate until biochemical resistance of plant cells
exists.
In spite of intensive investigations (sequential
extractions and specific extractants) on the prediction
of the availability of trace metals, it is not easy to
obtain good estimates of the general bioavailability of
a given trace element. However, based on results of
long-term experiments, some specific extractants, as
well as weak neutral salt solutions (e.g., 0.01 M
CaCl2) seem to be adequate to assess the impact of
trace elements on plants and soil bioactivity.
Plants reveal a great adaptation to the variable
composition of growth media, and have developed
several uptake mechanisms for a given nutrient under
deficiency conditions in soils, and can also exclude an
element at high external concentrations. However,
mechanisms involved in the exclusion processes are
much weaker than those developed by roots in the
absorption of deficient micronutrients. Thus, the excess
of trace metals in soils is a stronger stress to plants than
their deficiency. In general, plants readily take up trace
elements that are in the soil solution in either free ionic
or complexed forms. However, changes in the pH of the
root ambient solution and various root exudates can
significantly increase the availability of certain ele-
ments (Mortvedt et al., 1991). On the other hand, the
efflux of an excessive amount of zinc (possible also
other trace elements) from roots seems to be a protec-
tive mechanism in metal contaminated soils (Santa-
Maria and Cogliatti, 1998). Effects of root exudates on
the mobility of trace elements are variable, and as Zhao
et al. (2001) concluded, root exudates from plants that
hyperaccumulate metals (e.g., Thlaspi caerulescens)
are not involved in Zn and Cd accumulation.
Predicting the mobility in soil and bioavailabiliy of
trace elements has been a ’’hot topic’’ for years in both
agricultural and environmental studies. In spite of a
great instability and variability in trace element uptake
by plant roots, a number of extraction methods have
 A. Kabata-Pendias / Geoderma 122 (2004) 143–149 147

been suggested recently for the evaluation of their  Easy sorption from the alimentary track: Cd, Hg,
concentrations in soils. In general, they can be classi- Zn, I, B.
fied into separate groups as: acids, chelating agents,  Easy penetration trough placenta: Cd, Hg, Pb, Zn,
buffered salt solutions and unbuffered salt solutions. I.
Based on the results of long term experiments, neutral  Easy penetration through blood – brain barrier: Hg,
salt (of relatively low concentrations) extractions have B, Al, Pb.
been accepted as the best for simulating trace element  Damage to membranes, enzymes and various
concentrations in the soil solution and/or an element protein components: Hg, Pb, Cd, Zn, Ni, Se.
occurring in exchangeable fractions. The extracted  Damage to nucleic acid chain: Cd, Cu, Zn, Hg, Ni.
amounts of metals by these solutions are low and their
relative proportions range from < 1% to >20% of their The prediction of phytoavailability of trace ele-
total contents in soils (Table 4). ments is of crucial importance for the assessment of
The main aspects of the hazards to the environment environmental quality. The influence of soil parame-
through metal uptake by plants are presented by ters and plant absorption ability are the main factors
McLaughlin (2001), as follows: that govern phytoavailability of an element.
The most important master variables of soils which
 introduction of metals into the food chain, control element availability can be generalized as
 loss of vegetation cover induces through phyto- follows: pH and redox potential, texture, organic
toxicity, matter—quantity and quality, mineral composition,
 cycling of metals to surface soil horizons by temperature and water regime. Also interactions be-
tolerant plants to induce toxic effects on flora and tween chemical elements are known to influence the
fauna. phytoavailability of some trace elements. It is evident
that Ca, P, and Mg are often the main antagonistic
The environmental hazard of trace element pollu- elements in the absorption of several microcations.
tion depends on geochemical and biochemical prop- Agricultural practices of soil remediation are based
erties of a given element and are related to several most commonly on keeping a neutral soil pH and by
processes (Kabata-Pendias and Pendias, 2001) as amendments with materials having a high capacity to
follows: bind metals in possible slightly mobile fractions.
However, lime and phosphate (main remediation
 Easy bioaccumulation: (a) from aquatic environ- agents) application does not give always expected
ment: Hg, Cd, Pb, Cu, Zn, Sr; (b) from soil: Cd, effects, especially in the case of Cd (Jansson, 2002;
Zn, B, Ni, Sn, Cs, Rb. Lee and Doolittle, 2002). Also some synergistic
effects have been observed for selected pairs of
elements which can modify mobility/availability of
Table 4
the metal (Kabata-Pendias and Pendias, 2001).
Maximum amounts of metals (range in percent of total contents)
extracted from surface horizons of various soils after 24-h shaking There has been a great progress made in the
with different extractantsa understanding of mechanisms and external factors
Extractant Cu Zn Pb Mn Fe that control the uptake of trace elements by plants
0.02 M EDTA – Na 74 – 88 13 – 44 63 – 91 18 – 29 2–5
under various conditions. However, the prediction
1 M HCl 89 – 94 32 – 62 77 – 97 63 – 92 16 – 36 phytoavailability of trace elements, and especially in
0.1 M HCl 89 – 92 23 – 56 69 – 94 43 – 87 7 – 31 contaminated environments, is still very difficult.
1 M NH4NO3 2 – 16 1 – 25 1–2 1 – 16 0 There are several models to predict the phytoavail-
0.01 M CaCl2 0.3 – 7.8 0.5 – 22 0.3 – 2 0.8 – 15 0 ability of trace metals, especially of Cd, Zn, Cu and
1 M KCl 2–6 1 – 18 1–5 2 – 14 0
H2O 0.8 – 3.5 0.2 – 1 0.7 – 3 0.1 – 0.4 0
Pb (McLaughlin, 2001; Mortvedt et al., 1991), but
they are rather limited to a given plant and specific
EDTA: ethylenediaminetetraacetic acid (sodium salt).
DTPA: diethylenetriaminepentaacetic acid. growth conditions. Their application to crop plants
TEA: trietha. and field conditions, especially in the agricultural
a
After Karczewska (2002). landscape, is still uncertain.
148 A. Kabata-Pendias / Geoderma 122 (2004) 143–149
6. Assessing phytoavailable metals in soil
Methods used for the evaluation of the pool of
soluble (available) trace elements in soils are based
mainly on extractions by various solutions: (a) acids—
mineral acids at various concentrations, (b) chelating
agents—e.g., EDTA, DTPA [ + TEA], (c) buffered
salts—e.g., NH4OAc, (d) neutral salts CaCl2, MgCl2,
Sr(NO3)2, NH4NO3, and (e) other extractants, like
Coca Cola, proposed for routine soil testing. Some
other techniques like electrodialysis, diffusion through
membrane, diffusive gradient in thin film (DGT), and
bioindicators have been also proposed. However, since
a number of soil parameters and climatic factors have a
significant impact on the absorption of trace elements
by roots, any method used has to be related to a given
soil and plant conditions.
Desirable properties of these extractants are rela-
tively weak reactions with soil components and the
dissolution of elements related to the amount taken
up by most crop plants, and possible independence
of soil properties. In a view of all discussions and
evaluations of recent research results, there is
renewed interest in the earlier concept of Barber
(1984) of using extractants that simulate the natural
soil solution. These are solutions of neutral salts,
mainly CaCl2 in various concentrations (most fre-
quently 0.01 M). Also Häni and Gupta (1985) were
some of the first to propose the use of a neutral salt
solution to assess actual metal bioavailability. Houba
et al. (1999) recently confirmed the suitability of
0.01 M CaCl2 for the extraction of the bio-available
pool of metals. However, there is still a need to
evaluate analytical and sampling errors for a vide
range of soils, especially those contaminated by
metals originating from various sources, before these
methods will be finally recommended for regulatory
purposes.
7. Concluding remarks
The favourable environment for man is closely
related to chemical properties of soils, and in partic-
ular to adequate and safe contents of trace elements.
Assessment criteria and application guidelines for
trace elements in soils are now objectives of legisla-
tion actions in most countries.
The limits for metal loading rates to soils should
consider general ecotoxicity, phytotoxicity, transfer to
animals and risk to the human population, based on
pathways such as direct soil ingestion, contamination
of plant food and pollution of waters These limits
should also consider the long-term phytoavailability
of metals in soils amended with various wastes.
Requirements for good/minimum soil quality stand-
ards should be related to soil type and land use. All
master variables, both biotic and abiotic should be
considered in the ecological and health relevance of
the trace element status in soils.
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