Environmental Pollution 144 (2006) 93e100www.elsevier.com/locate/envpol

A comparison of phytoremediation capability of selected plantspecies for given trace elements

Zuzana Fischerova, Pavel Tlustos*, Jirina Szakova, Kornelie Sichorova

Department of Agrochemistry and Plant Nutrition, Czech University of Agriculture in Prague, Kamycka 957, 165 21 Prague 6dSuchdol,Czech Republic

Received 1 June 2005; accepted 8 December 2005

Selected accumulator trees grown on medium contaminated soil may have remediation capacity similar tohyperaccumulator species.

Abstract

In our experiment, As, Cd, Pb, and Zn remediation possibilities on medium contaminated soil were investigated. Seven plant species witha different trace element accumulation capacity and remediation potential were compared. We found good accumulation capabilities and reme-diation effectiveness of Salix dasyclados similar to studied hyperaccumulators (Arabidopsis halleri and Thlaspi caerulescens). We have noticedbetter remediation capability in willow compared to poplar for most of the elements considered in this experiment. On the contrary, poplar spe-cies were able to remove a larger portion of Pb as opposed to other species. Nevertheless, the removed volume was very small. The elementsfound in plant biomass depend substantially on the availability of these elements in the soil. Different element concentrations were determined innatural soil solution and by inorganic salt solution extraction (0.01 mol L�1 CaCl2). Extracted content almost exceeded the element concentra-tion in the soil solution. Element concentrations in soil solution were not significantly affected by sampling time.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Remediation; Hyperaccumulator; Willow; Poplar; Soil solution; Accumulation

1. Introduction

Phytoremediation is one of the environmental friendly tech-nologies that uses plants to clean up soil from trace elementcontamination. The uptake and accumulation of pollutantsvary from plant to plant and also from species to specieswithin a genus (Singh et al., 2003). Proper selection of plantspecies for phytoremediation plays an important role in the de-velopment of remediation methods (decontamination or stabi-lization), especially on low-or-medium-polluted soils (Saltet al., 1995). There are several distinct groups of plant speciesaccording to their trace element accumulation capability.These are: excluders with avoidance (or restriction) mecha-nism for element uptake, highly sensitive indicators lacking

* Corresponding author. Tel.: þ420 22 438 2733; fax: þ420 23 438 1801.

E-mail address: tlustos@af.czu.cz (P. Tlustos).

0269-7491/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2006.01.005

a protection mechanism, and accumulators with mechanismsof metal tolerance and accumulation capability in above-ground biomass. A particular sub-group within the accumula-tors is represented by the hyperaccumulators (Adriano, 2001).Hyperaccumulators are plants commonly grown on metallifer-ous soils and able to complete their life cycle without anysymptoms of metal phytotoxicity (Baker et al., 2000). Unfor-tunately, these plants usually produce less biomass than otherplant species. Hyperaccumulation limits were defined withthe respect to individual metal as 100 mg kg�1 of Cd,1000 mg kg�1 of Pb and 10,000 mg kg�1 of Zn of plant dryweight (Baker and Brooks, 1989; Baker et al., 2000). Thethreshold value for As has not been defined yet.

Just recently, plant species such as fern (Pteris vittata), witha recognized capability of As phytoextraction, were found (Maet al., 2001). P. vittata accumulates most of arsenic into youngleaves, less is deposited into old leaves, rhizomes and roots,respectively. Fitz et al. (2003) estimated that approximately

94 Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

2580 mg kg�1 of As were accumulated in young leaves com-pared to 119 mg kg�1 in roots. This fern is able to accumulate1442e7526 mg kg�1 of As in shoots when it is grown on con-taminated soil (Ma et al., 2001).

As a result of low levels of cadmium found in soil as wellas in plant biomass, the lowest hyperaccumulation thresholdvalue for Cd was defined. Only few plant species with thisability were identified. These are: Thlaspi caerulescens(Schwartz et al., 2003) containing more than 1000 mg kg�1

of Cd in leaves (Baker et al., 2000) and Arabidopsis halleriwith a shoot concentration of 157 mg kg�1 (Bert et al., 2003).

Lead has very low mobility in soils as well as in plant tissues.There are some plant species classified as hyperaccumulators,which exceeding the hyperaccumulation limit, as describedby Baker and Brooks (1989). Among them, Thlaspi rotundifo-lium containing up to 8200 mg kg�1 of Pb and Thlaspi caerules-cens with a shoot concentration of 2,740 mg kg�1 whengrowing on contaminated soil are the typical ones (Baker andBrooks, 1989; Baker et al., 2000).

Zinc is an essential trace element for plants; however, itcould be toxic in high concentrations. Usually, concentrationin plant biomass ranges from 10 to 150 mg kg�1 of dry weight,nevertheless zinc concentration for some plant species staysaround 1000 mg kg�1 dry weight (Baker and Brooks, 1989;Mulligan et al., 2001). For instance, zinc-hyperaccumulatingplants are Arabidopsis halleri, Thlaspi caerulescens, Violacalaminaria and several other species from the genus Thlaspi(Baker and Brooks, 1989; Sarret et al., 2002). Plant specieswith tolerance to high concentration of trace elements belongpreferentially to the families: Caryophyllaceae, Brassicaceae,Cyperaceae, Poaceae, Fabaceae, and Chenopodiaceae(Kabata-Pendias and Pendias, 2001). Thlaspi caerulescens isknown as a Cd and Zn hyperaccumulator which can growon highly contaminated soils without showing any symptomsof phytotoxicity or changes in aboveground biomass yield(Gove et al., 2002; Zhao et al., 2003; Keller and Hammer,2004; Sterckeman et al., 2004). While cadmium shoot concen-trations did not vary in time, zinc concentration gradually de-creased during the vegetation period (Perronnet et al., 2003).

Besides hyperaccumulators there are plant species likeSalix viminalis (which takes up large portion of Cd and Zn),Brassica juncea (Pb), Lolium perenne (Pb), Zea mays (Pb),Helianthus annuus (Pb, Cu), or others, characterized by highcontent of heavy metals in biomass and good remediation ca-pacity (Schmidt, 2003; Bricker et al., 2001). A large numberof species and hybrids of Salix spp. suggest wide genetic var-iability within the genus and some species are known to colo-nize contaminated soil. For example Salix alba, S. dasyclados,S. viminalis, S. cinerea, and S. caprea naturally colonize pol-luted dredged sediment disposal sites (Vandecasteele et al.,2002; Pulford and Watson, 2002; Klang-Westin and Eriksson,2003). In these experiments, the willow plants were able to ac-cumulate 4.1 mg kg�1 of Cd in stems and 7.3 mg kg�1 of Cdin leaves. Some willow or poplar varieties do not retain ele-ments in roots but transfer them to aboveground planttissues (Robinson et al., 2000; Pulford and Watson, 2002;Vyslou�zilova et al., 2003). The advantage of these species is

their greater harvestable biomass compared to most hyperac-cumulators with only small aboveground biomass (Cobbettand Meagher, 2002).

Identification and quantification of element fractions associ-ated with individual soil components could lead to a better char-acterization of potentially toxic plant-available elements and toan understanding of the behavior of these elements in soil. Thefollowing order of extractability of individual elements wasobtained by sequential extraction procedure (Szakova et al.,1999): As residual > bound in FeeMn oxides > organicallybound > exchangeable > water soluble; Cd bound in FeeMnoxides > exchangeable > residual > organically bound > -water soluble; Zn residual > bound in FeeMn oxides > organi-cally bound > exchangeable > water-soluble. Most of arsenicand lead have low mobility and are bound to residual soil frac-tion whereas residual cadmium usually does not exceed 50%of total cadmium concentration (Mulligan et al., 2001; Wenzelet al., 2002). Gray et al. (2000) applied sequential extraction pro-cedure for fractionation of cadmium in a set of New Zealandsoils resulting in mean proportions of Cd present in individualfractions in the following order: residual (38%) > organic(35%) > > amorphous oxide (13%) > crystalline oxide(12%) > exchangeable (3%). The relatively high Cd ratio inorganic fraction, and rather low proportion of this element inthe two oxide fractions were explained by the high content oforganic carbon in association with low iron content in the ana-lyzed soils. Water soluble and exchangeable fractions (usually0.5e3.2% and 4e18% of total Cd and Zn content, respectively)characterize the most mobile metal species in soils. The elementpool bound to FeeMn oxides and organically bound can bemobilized by changing soil physicochemical properties. Thetransfer of trace elements from the soils to the plant dependson three factors: the total concentration of potentially availableelement (quality factor), the activity as well as the ionic ratio ofelements in the soil solution (intensity factor), and the rate ofelement transfer from solid to liquid phases and to plant roots(reaction kinetics). Easily soluble forms of elements are themost dangerous for the environment. Because there is a strongcorrelation between soluble trace element concentrations inthe soil as well as in plants, several countries passed legislationestablishing quality standards based on soluble trace elementconcentrations in the soil (Schmidt, 2003).

Various extraction procedures (using e.g. CaCl2, Ca(NO3)2,NaNO3, BaCl2 solutions) were described for the determinationof mobile and bioavailable portions of elements in soils. Theextractability of elements depends on the nature of the extrac-tant, the source of soil pollution, and the nature of the soil(Moral et al., 2002). Besides classical soil extraction tech-niques, direct sampling of soil solution plays an importantrole in soil available trace element concentrations estimation.In situ sampling is preferred among other techniques becauseof possible physicochemical and biological transformation ofelements during sampling, storage and handling. Natural soilsolution contains water with dissolved colloids, soluble com-plexes, metal compounds, and element ions (Adriano, 2001).The knowledge of soil solution composition is essential to un-derstand trace element plant uptake. Trace elements content in

95Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

soil solution immediately defines available concentration ofmetals for the plant. Element concentration in soil solutionvaries according to soil type, time, vegetation cover, activityof microorganisms, water regime, and soil heterogeneity.Rainfall, evaporation, and plant transpiration can change traceelement concentrations in soil solution, whereas variations inthe concentration of major ions (Ca2þ, Mg2þ, Kþ, Naþ,NO3�, and others) are much smaller. Nevertheless, the range

of trace element concentrations, as measured in various soilsolutions, is reasonably comparable (Kabata-Pendias andPendias, 2001). Wenzel et al. (2002) determined relativelysmall seasonal variation of As in soil solution. However, theresults of soil solution measurements are affected by lysimeteror suction cup material and its element adsorption ability(Andersen et al., 2002; Wenzel et al., 1997).

The aim of this work was to compare trace element accu-mulation capacity and remediation capability of selected plantspecies grown on medium contaminated soil and to assesschanges in the concentration of soil-available metals. Wehave studied two hyperaccumulators and five potential accu-mulators with high biomass production. Plant accumulationcapacity was calculated as weighed average of trace elementtotal concentration in aboveground plant structures with re-spect to total yield of selected parts of shoot. Remediation ca-pacity represents an average ratio of trace element extractedby plants from total element concentration in soil per onegrowing season. It was calculated as total element uptake byaboveground biomass divided by total element concentrationin soil with respect to volume of experimental soil. Further-more, changes of available trace element concentration insoil solution during the vegetative growth stage were evaluatedand compared with traditional mild soil extraction procedure.

2. Materials and methods

2.1. Vegetation experiment

Plant accumulation capacity and remediation capability were tested in

a two-year pot experiment. Pots were placed outdoors and were partially cov-

ered to protect them from the rainfall. We used anthropic contaminated Cam-

bisol from the Pribram area (Central Bohemia, Czech Republic) containing

28 mg kg�1 As, 5.46 mg kg�1 Cd, 956 mg kg�1 Pb, and 279 mg kg�1 Zn. De-

tailed characteristics of this site were described in Sichorova et al. (2004). Five

kilograms of dry homogenized topsoil were fertilized with 0.5 g N, 0.16 g P,

and 0.4 g K and applied to each pot. In addition, plants were once or twice

fertilized during the vegetative period with a complex of macro- and micro-

nutrients. Plants were selected from two groups: hyperaccumulatorsd

Arabidopsis halleri (L.) Hayek and Thlaspi caerulescens J. et C. Presl; and

accumulator trees with a great biomass productiondSalix � smithiana Willd.

cf. dasyclados, Salix � dasyclados Vimm., Salix caprea L., Populus

trichocarpa Torr. et Gray � koreana Rehd., Populus nigra L. � maximowiczii

Henry. All treatments involved five replicates. The plant species tested in this

experiment originated from model experimental conditions. These are: T.

caerulescens from Ganges area (France), A. halleri and S. caprea from

BOKU in Vienna (Austria), and clones of S. smithiana, S. dasyclados, P.

trichocarpa and P. nigra from Silva Tarouca Research Institute for Landscape

and Ornamental Gardening in Pruhonice (Czech Republic) (Weger and

Havlı�ckova, 2002). In both years, aboveground biomass of studied plant spe-

cies was harvested and separated in different plant structures (leaves and

stems) whereas one part of experimental pots was harvested including roots.

Soil solution was collected from the pots three times during the vegetative

growth stage to investigate actual concentration of available trace elements in

the soil in a two-year period. We used specialized plastic suction cups (D.I.

Gottfried Wieshammer, Wien, Austria), which were applied to selected treat-

ments (with three replicates) at the beginning of the experiment to obtain soil

solution. Selected pots with installed suction cups were watered with deion-

ized water to full water holding capacity one day before suction and left for

24 h to reach equilibrium. Ten milliliters of soil solution from each pot was

always sampled and immediately analyzed for As, Cd, Pb, and Zn

concentrations.

2.2. Laboratory procedure

After harvest, plants were dried at 65 � C, homogenized, and decomposed

by modified dry ashing procedure with the mixture of oxidizing gases

(O2 þ O3 þ NOx) in Apion Dry Mode Mineralizer (Tessek, Czech Republic)

at 400 �C for 10 h. The ash was dissolved in 20 ml 1.5% HNO3 (Miholova

et al., 1993). Soil samples were air-dried and their available trace element con-

tent was determined by extraction with 0.01 mol L�1 CaCl2 (Novozamsky

et al., 1993).

Trace elements (As, Cd, Pb, and Zn) concentrations were determined in

plant digests, soil extracts, and soil solution samples by inductively coupled

plasma optical emission spectrometry (ICP-OES, Varian Vista Pro, Varian,

Australia). Certified reference materials RM NCS DC 73350 Poplar leaves

and RM 7001 Light Sandy Soil were used to assess quality of analytical

data. Statistical analyses were made using software Statgraphics Plus v. 5.0

with ANOVA test (a ¼ 0.05).

3. Results and discussion

3.1. Trace elements accumulation by plants

All the plant species tested in the experiment were grownon medium contaminated soil showing no visible symptomsof toxicity. We calculated the weighted mean of metal concen-tration in shoots with respect to element concentrations in par-ticular plant structures and yields in dry weight. From theseresults, we compared accumulation ability of tested plant spe-cies. Both hyperaccumulators confirmed their extremely hightrace element accumulation capacity compare to other testedspecies (Table 1). Although they never exceeded the hyperac-cumulation threshold value, they were able to take up signifi-cantly higher concentrations of As, Cd, Pb, and Zn thanplanted trees. This was particularly observed in the case ofAs and Zn. In general, both hyperaccumulators took up a sig-nificantly higher trace element dose compared to other plantspecies. Comparing among the fast growing trees, willows ac-cumulated usually more Cd and Zn than poplars, especially S.dasyclados. On the other hand, poplar trees took up more leadcompared to willows. Concerning arsenic, no significant dif-ferences were observed among willow and poplar species.

Detailed evaluation of the data showed that only lead con-centration in T. caerulescens was significantly higher than inother plant species. Concentration of Pb in A. halleri biomassdid not statistically differ from concentrations of Pb in trees.Cadmium content in T. caerulescens significantly exceededthe levels of Cd in other species including A. halleri. Concen-tration of Cd, which was determined in aboveground biomassof A. halleri, did not differ from S. dasyclados and S. capreaCd concentrations but significantly exceeded S. smithiana, P.trichocarpa, and P. nigra concentrations. This corresponds

96 Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

Table 1

Average content of elements in aboveground biomass (x in mg kg�1, n ¼ 10) and annual remediation factor (Rf in %)

Species As Cd Pb Zn

x Rf x Rf x Rf x Rf

A. halleri 6.07a 0.067a 82.3a 4.75abc 21.9a 0.008ab 2746a 2.92a

T. caerulescens 5.30a 0.028b 271b 7.55cd 57.6b 0.010ab 1500b 0.963d

S. smithiana 1.25b 0.035b 23.6c 3.36a 6.84a 0.005a 432c 1.17cd

S. dasyclados 0.964b 0.033b 41.1ac 8.10d 10.9a 0.012b 591c 2.24ab

S. caprea 1.08b 0.038b 32.8ac 6.38cd 8.14a 0.008ab 475c 1.79bc

P. trichocarpa 0.825b 0.039b 20.4c 5.0abc 17.3a 0.024c 337c 1.61bcd

P. nigra 0.918b 0.047ab 17.3c 4.58ab 16.7a 0.025c 344c 1.77bc

Dmin 1.85 0.023 50.2 2.66 19.1 0.005 401 0.786

The averages marked by the same letter did not significantly differ at a ¼ 0.05 within individual columns.

with Robinson et al. (2000) concluding that willows are able toaccumulate more Cd than poplar plants. Concentrations of ar-senic and zinc in both hyperaccumulators significantly ex-ceeded concentrations of these elements in trees and nostatistical differences among element concentrations in the an-alyzed tree species were determined. From this point of viewthere could be more advantageous to plant hyperaccumulatorsthan to other plant species due to high concentration of ele-ments in the aboveground biomass. We have determined sim-ilar concentrations of each element in shoots of trees in bothyears while in biomass of A. halleri the element concentrationsdecreased in the second vegetation period. Likewise, in leavesof T. caerulescens the Pb levels decreased while Cd and Znlevels increased in the second year (data not showed). It ispartly in accordance with Keller and Hammer (2004) who con-cluded a significant increase in the concentration of Zn in theleaves in three following T. caerulescens croppings, but theydid not register changes in the concentration of Cd in plantsgrown on unamended soil.

3.2. Remediation capacity

Remediation technologies appoint to remove the majority ofelements from contaminated soil. The total element content inaboveground biomass is only one of the factors. The most im-portant component is probably the remediation factor (Rf),which represents percentage of element removed per yearfrom a determined volume of soil with the respect to plant ele-ment concentration and plant yield. The calculation was alreadypublished in Vyslou�zilova et al. (2003) or Zhao et al. (2003). Inour experiment, the plant species with lower element concentra-tion in shoots compensated the remediation effectiveness bygreat biomass production compared to plant species with higherelement concentration and low biomass production (Table 1).Despite statistically significant differences in calculated reme-diation factors there was practically no difference in remedia-tion efficiency between hyperaccumulators and selected trees,especially for S. dasyclados. The use of these species mayhave a similar effect. Remediation factor of willow variedwith plant genotype. Greger and Landberg (1999) concludedthat some varieties of Salix spp. have a remediation capacityof about five times higher than hyperaccumulators

(T. caerulescens or Alyssum murale) due to the high biomassproduction and transport of Cd and Zn to shoots. Ratio of ele-ments removed from the soil by plants proportionally decreasedwith increasing total content of element in soil. This is partly inaccordance with our results. We registered similar or a slightlyhigher remediation capacity for S. dasyclados (optionally pop-lar trees for Pb) compared to hyperaccumulators. In contrast,Keller et al. (2003) considered T. caerulescens as a more effi-cient species in trace element removal than Salix viminalis orNicotiana tabacum due to higher total element concentrationin aboveground biomass. On the other hand, willow (Salixviminalis), showed a great remediation potential, as well.Klang-Westin and Eriksson (2003) observed higher content ofCd in leaves and stems of smaller willow plants compared tomuch bigger yielding plants. Schwartz et al. (2003) observedthe same effect in T. caerulescens shoots. Obviously there areno significant differences in Thlaspi and selected Salix speciesregarding remediation capability.

We investigated element shoot/root accumulation ratio toassess its transport within the plant tissue. Fig. 1 showsa good likelihood of all tested species to transport Cd andZn from roots to aboveground biomass. All species depositAs and Pb preferentially in roots. The highest shoot/root Cdratio was found in A. halleri, S. dasyclados, P. trichocarpaand P. nigra. Significantly higher transport of Zn was ob-served in both poplar species compared to other ones. Thisis in accordance with results of many other authors that de-scribed the highest concentration of Cd and Zn in poplar orwillow leaves compared to other plant structures (Pulford

0

1

2

3

As Cd Pb Zn

AH TC SS SD SC PT PN

Fig. 1. Average element accumulation shoot/root ratio of different plant spe-

cies (n ¼ 4).

97Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

and Watson, 2002). We are able to conclude that poplar treesare indeed capable of transport Cd and Zn to shoots, but theirremediation factor is lower in contrast to both hyperaccumula-tors and S. dasyclados. From the practical point of view, it iseasier to use trees because of their greater biomass productionand easier treatment, harvest, and later manipulation with bio-mass compared to small hyperaccumulators. Tree utilization insoil remediation has more advantages than herb planting.Trees, such as poplars, are able to transpire more water, theycan get water from deeper soil horizons, and they have betterregeneration capability than herbs (most of hyperaccumulatorspecies), especially in spring revegetation (Pierzynski, 1997).

3.3. Available content of metals in soil

Many authors have realized the relationship between traceelement soluble concentrations in the soil and in plants(Schmidt, 2003). Available concentration of metals in thesoil is usually determined using 0.01 mol L�1 CaCl2 or1 mol L�1 NH4NO3 extraction (Hornburg and Brummer,1993; Degryse et al., 2003; Pueyo et al., 2004). Kabata-Pen-dias and Pendias (2001) compared available trace elementcontent from several soils measured in 0.01 mol L�1 CaCl2 so-lutions and soil solutions from porous suction cups. Extract ofCaCl2 contained 21e180 mg L�1 of Zn and presence of As,Cd, and Pb was not detected. Soil solution from suctioncups contained 4e12 mg L�1 of As, 0.2e300 mg L�1 of Cd,0.6e63 mg L�1 of Pb, and 4e17,100 mg L�1 of Zn. Wenzelet al. (2002) determined 0.3e101.4 mg L�1 of As measuredin soil solution according to soil type, horizon, and depth. Inour experiment we determined concentration of elements inCaCl2 solution at different intervals 12.2e31.8 mg L�1 of

As, 6.1e72.6 mg L�1 of Cd, 200e1009 mg L�1 of Pb, and120e1236 mg L�1 of Zn. Soil solutions extracted from thepots were used to measure metal concentrations in the rangeof 25.1e35.6 mg L�1 of As, 1.6e8.2 mg L�1 of Cd, 16.1e100 mg L�1 of Pb, and 31.6e838 mg L�1 of Zn, respectively.However, this comparison is the critical point. As it is ex-pected, the data published in literature and element concentra-tions measured in this experiment are weakly comparablebecause of extractions and analyses provided in specific soilconditions and/or experimental parameters of individual trials.

In total six soil solution samples for each of the two vege-tation periods (three suctions per year) were carried in order todetermine changes in available concentration of trace elementsin the soil during the vegetative growth. Furthermore, a com-parison between element concentration in soil solution and el-ement concentrations determined in traditional soil extracts(0.01 mol L�1 CaCl2 extraction) was conducted. Soil samplesintended for laboratory procedure (CaCl2 extraction) were re-leased at the end of the vegetative period. Control variant lack-ing plant vegetation cover was used for this determination. Inmost cases, element content determined in CaCl2 extractionexceeded the concentration measured in soil solution for allstudied plant species (Fig. 2). Only a few exceptions did notcorrelate with these results. From heavy metals only Zn con-centration in the control treatment did not follow this pattern.A slightly different situation was observed for arsenic. Theconcentration of arsenic in CaCl2 extract overstepped (not sig-nificantly) As content in soil solution only in S. smithianatreatment. Significant differences of Cd and Pb concentrationsin soil solution as well as CaCl2 extract raises concerns aboutapplicability of CaCl2 extraction to determine available con-tent of these elements in the soil. Moreover, significant

Arsenic

0

10

20

30

40

TC SS SD SC PN control TC SS SD SC PN control

TC SS SD SC PN controlTC SS SD SC PN control

Soil solution CaCl2

Soil solution CaCl2 Soil solution CaCl2

Soil solution CaCl2

Cadmium

0

20

40

60

Lead623 925

0

100

200

300

400

g

L-1

g

L-1

g

L-1

Zinc1.05

0.0

0.2

0.4

0.6

0.8

1.0

mg

L-1

Fig. 2. Differences between trace elements concentrations in soil solution and in CaCl2 extract (n ¼ 6).

98 Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

differences in element extractability by individual extractingagents were documented by Hornburg et al. (1995) who deter-mined higher content of metals in CaCl2 extract compared toNH4NO3 solution.

Kabata-Pendias and Pendias (2001) found very similar con-tent of trace elements in soil solution from various soils andwe measured more or less similar concentrations of trace ele-ments in soil solution from different plant treatments. Changesin element available portion in soil solution of different plantspecies were evaluated with respect to time. Zhang et al.(1998) described the resupply of trace elements available frac-tions in the soil. In our measurements we were able to recorda decrease in Cd and Zn concentration compared to the controlassay for most of the time during the experiment (Fig. 3, datafor Zn is not shown) given by plant trace element uptake asdescribed also by Szakova et al. (2003). Relatively constantconcentration of elements in the soil solution during the veg-etative growth confirms the theory of continuous element re-supply. On the third suction (at the end of the firstvegetation year) of the treatment with S. dasyclados we cansee a sharp increase in the concentration of Cd in soil solution.This was probably caused by lower plant element uptake withconstant element resupply processes in the soil. In the secondyear there were no strong deviations like this one, probablydue to climatic conditions (warm summer in the first yearand cold weather in the second year).

Cadmium

0

10

20

30

1 2 3 4 5 6

1 2 3 4 5 6

Suction Nr.TC SS SD SC PN control

TC SS SD SC PN control

Lead

0

50

100

150

200

Suction Nr.

g

L-1

g

L-1

Fig. 3. Time dependent changes of trace elements concentrations in soil solu-

tion affected by different plant species (suction 1e3, first year; 4e6, second

year; n ¼ 3). AH, Arabidopsis halleri; TC, Thlaspi caerulescens; SS, Salix

smithiana; SD, Salix dasyclados; SC, Salix caprea; PT, Populus trichocarpa;

PN, Populus nigra.

At the end of both vegetative periods, the lead content insoil solution of different plant species slightly increased.This was probably caused by a restriction in plant element up-take. All tested plant species, contained slightly higher con-centrations of Pb in soil solution compared to the controltreatment. Soil solution of P. nigra contained a higher Pb con-centration than other species including the control treatmentall the time. This was probably caused by root exudates witha wide range of organic and inorganic substances, which inev-itably led to changes in soil biochemical and physical proper-ties (Walker et al., 2003) and metal mobilization. Poplar treesare able to remediate relatively high ratio of Pb, as describedabove. We calculated the best remediation effectiveness forboth poplar species compared to other species analyzed. Eval-uation of arsenic content showed only possible decreases inthe concentration of this element between the first and thesecond year of cropping. There are no evident trends in plantelement uptake or mobilization in the soil (data not shown).

Our results showed a significant impact of plant species andits capability to take up trace elements from the soil and accu-mulate them in aboveground biomass. Some plant species areable to influence the available pool of elements in the soil dueto root exudates and are also capable of removing trace ele-ments compared to other species. These results come fromthe pot experiment. In general, plants grown in pot experimentusually contain higher concentrations of trace elements thanplants grown in the field. Plants grown in the field showeda 20% decrease of remediation efficiency compared to theplants from pot experimental conditions (Schmidt, 2003). Inspite of this it is necessary to understand the principles of phy-toremediation and the processes that occur under regulatedconditions prior to use in contaminated areas.

4. Conclusions

Widespread need to remediate soils in areas contaminatedwith high concentrations of trace elements generates interestabout environmental friendly remediation technologies. Phy-toremediation uses plants to decrease soil pollution to an ac-ceptable level. It is necessary to find plant species witha good accumulation capacity and remediation capability.Seven plant species with different yield and accumulation abil-ity were tested in our experiment for their remediation charac-teristics. We have confirmed hyperaccumulation possibility ofA. halleri and T. caerulescens for Cd and great accumulationability for other studied elements. Very good accumulationwas determined in tested trees, too. In particular, willowS. dasyclados compensated lower metal content in shootswith higher biomass production compared to hyperaccumula-tors, which have higher element content but lower above-ground biomass resulting in similar remediation capability.Although poplar trees showed the best willingness to transportCd and Zn from roots to shoots, their remediation potentialdoes not achieve S. dasyclados or hyperaccumulators level.Available concentrations of trace elements in soil measuredin direct soil solution were observed, too. We have recordedno significant differences of element concentrations in soil

99Z. Fischerova et al. / Environmental Pollution 144 (2006) 93e100

solution in time. Results indicate that plant character and rootexudates have preferential effects on trace elements uptakeand accumulation by plants.

Acknowledgements

Financial support for these investigations was provided byProjects No. MSM 6046070901 and COST OC 631 002.

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