A comparison of phytoremediation capability of selected plant

Environmental Pollution 144 (2006) 93e100 www.elsevier.com/locate/envpol

A comparison of phytoremediation capability of selected plant species for given trace elements Zuzana Fischerova´, Pavel Tlustosˇ*, Jirˇina Sza´kova´, Kornelie Sˇichorova´ Department of Agrochemistry and Plant Nutrition, Czech University of Agriculture in Prague, Kamy´cka´ 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 to hyperaccumulator species.

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

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

1. Introduction Phytoremediation is one of the environmental friendly technologies that uses plants to clean up soil from trace element contamination. The uptake and accumulation of pollutants vary from plant to plant and also from species to species within a genus (Singh et al., 2003). Proper selection of plant species for phytoremediation plays an important role in the development of remediation methods (decontamination or stabilization), especially on low-or-medium-polluted soils (Salt et al., 1995). There are several distinct groups of plant species according to their trace element accumulation capability.

These are: excluders with avoidance (or restriction) mechanism 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. Tlustosˇ).

0269-7491/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2006.01.005

a protection mechanism, and accumulators with mechanisms of metal tolerance and accumulation capability in aboveground biomass. A particular sub-group within the accumulators is represented by the hyperaccumulators (Adriano, 2001).

Hyperaccumulators are plants commonly grown on metalliferous soils and able to complete their life cycle without any symptoms of metal phytotoxicity (Baker et al., 2000). Unfortunately, these plants usually produce less biomass than other plant species. Hyperaccumulation limits were defined with the 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 dry weight (Baker and Brooks, 1989; Baker et al., 2000). The threshold value for As has not been defined yet.

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

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2580 mg kg 1 of As were accumulated in young leaves compared to 119 mg kg 1 in roots. This fern is able to accumulate 1442e7526 mg kg 1 of As in shoots when it is grown on contaminated soil (Ma et al., 2001).

As a result of low levels of cadmium found in soil as well as in plant biomass, the lowest hyperaccumulation threshold value for Cd was defined. Only few plant species with this ability 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 halleri with 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 described

by Baker and Brooks (1989). Among them, Thlaspi rotundifolium containing up to 8200 mg kg 1 of Pb and Thlaspi caerulescens with a shoot concentration of 2,740 mg kg 1 when growing on contaminated soil are the typical ones (Baker and Brooks, 1989; Baker et al., 2000).

Zinc is an essential trace element for plants; however, it could be toxic in high concentrations. Usually, concentration in plant biomass ranges from 10 to 150 mg kg 1 of dry weight, nevertheless zinc concentration for some plant species stays around 1000 mg kg 1 dry weight (Baker and Brooks, 1989; Mulligan et al., 2001). For instance, zinc-hyperaccumulating plants are Arabidopsis halleri, Thlaspi caerulescens, Viola calaminaria and several other species from the genus Thlaspi (Baker and Brooks, 1989; Sarret et al., 2002). Plant species with tolerance to high concentration of trace elements belong preferentially to the families: Caryophyllaceae, Brassicaceae, Cyperaceae, Poaceae, Fabaceae, and Chenopodiaceae (Kabata-Pendias and Pendias, 2001). Thlaspi caerulescens is known as a Cd and Zn hyperaccumulator which can grow on highly contaminated soils without showing any symptoms of 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 concentrations did not vary in time, zinc concentration gradually decreased during the vegetation period (Perronnet et al., 2003).

Besides hyperaccumulators there are plant species like Salix 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 high content of heavy metals in biomass and good remediation capacity (Schmidt, 2003; Bricker et al., 2001). A large number of species and hybrids of Salix spp. suggest wide genetic variability within the genus and some species are known to colonize contaminated soil. For example Salix alba, S. dasyclados, S. viminalis, S. cinerea, and S. caprea naturally colonize polluted 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 accumulate 4.1 mg kg 1 of Cd in stems and 7.3 mg kg 1 of Cd in leaves. Some willow or poplar varieties do not retain elements in roots but transfer them to aboveground plant tissues (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 hyperaccumulators with only small aboveground biomass (Cobbett and Meagher, 2002).

Identification and quantification of element fractions associated with individual soil components could lead to a better characterization of potentially toxic plant-available elements and to an understanding of the behavior of these elements in soil. The following order of extractability of individual elements was obtained by sequential extraction procedure (Sza´kova´ et al., 1999): As residual > bound in FeeMn oxides > organically bound > exchangeable > water soluble; Cd bound in FeeMn oxides > exchangeable > residual > organically bound > water soluble; Zn residual > bound in FeeMn oxides > organically bound > exchangeable > water-soluble. Most of arsenic and lead have low mobility and are bound to residual soil fraction whereas residual cadmium usually does not exceed 50% of total cadmium concentration (Mulligan et al., 2001; Wenzel et al., 2002). Gray et al. (2000) applied sequential extraction procedure for fractionation of cadmium in a set of New Zealand soils resulting in mean proportions of Cd present in individual fractions in the following order: residual (38%) > organic (35%) > > amorphous oxide (13%) > crystalline oxide (12%) > exchangeable (3%). The relatively high Cd ratio in organic fraction, and rather low proportion of this element in the two oxide fractions were explained by the high content of organic carbon in association with low iron content in the analyzed soils. Water soluble and exchangeable fractions (usually 0.5e3.2% and 4e18% of total Cd and Zn content, respectively) characterize the most mobile metal species in soils. The element pool bound to FeeMn oxides and organically bound can be mobilized by changing soil physicochemical properties. The transfer of trace elements from the soils to the plant depends on three factors: the total concentration of potentially available element (quality factor), the activity as well as the ionic ratio of elements in the soil solution (intensity factor), and the rate of element transfer from solid to liquid phases and to plant roots (reaction kinetics). Easily soluble forms of elements are the most dangerous for the environment. Because there is a strong correlation between soluble trace element concentrations in the soil as well as in plants, several countries passed legislation establishing quality standards based on soluble trace element concentrations in the soil (Schmidt, 2003).

Various extraction procedures (using e.g. CaCl2, Ca(NO3)2, NaNO3, BaCl2 solutions) were described for the determination of mobile and bioavailable portions of elements in soils. The extractability of elements depends on the nature of the extractant, the source of soil pollution, and the nature of the soil (Moral et al., 2002). Besides classical soil extraction techniques, direct sampling of soil solution plays an important role in soil available trace element concentrations estimation.

In situ sampling is preferred among other techniques because of possible physicochemical and biological transformation of elements during sampling, storage and handling. Natural soil solution contains water with dissolved colloids, soluble complexes, metal compounds, and element ions (Adriano, 2001).

The knowledge of soil solution composition is essential to understand trace element plant uptake. Trace elements content in

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

soil solution immediately defines available concentration of metals for the plant. Element concentration in soil solution varies according to soil type, time, vegetation cover, activity of microorganisms, water regime, and soil heterogeneity.

Rainfall, evaporation, and plant transpiration can change trace element concentrations in soil solution, whereas variations in the concentration of major ions (Ca2þ, Mg2þ, Kþ, Naþ, NO 3 , and others) are much smaller. Nevertheless, the range of trace element concentrations, as measured in various soil solutions, is reasonably comparable (Kabata-Pendias and Pendias, 2001). Wenzel et al. (2002) determined relatively small seasonal variation of As in soil solution. However, the results of soil solution measurements are affected by lysimeter or 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 accumulation capacity and remediation capability of selected plant species grown on medium contaminated soil and to assess changes in the concentration of soil-available metals. We have studied two hyperaccumulators and five potential accumulators with high biomass production. Plant accumulation capacity was calculated as weighed average of trace element total concentration in aboveground plant structures with respect to total yield of selected parts of shoot. Remediation capacity represents an average ratio of trace element extracted by plants from total element concentration in soil per one growing season. It was calculated as total element uptake by aboveground biomass divided by total element concentration in soil with respect to volume of experimental soil. Furthermore, changes of available trace element concentration in soil solution during the vegetative growth stage were evaluated and 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 covered to protect them from the rainfall. We used anthropic contaminated Cambisol 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. Detailed characteristics of this site were described in Sˇichorova´ 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 micronutrients. 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 Pru˚honice (Czech Republic) (Weger and Havlı´ ckova´, 2002). In both years, aboveground biomass of studied plant species was harvested and separated in different plant structures (leaves and stems) whereas one part of experimental pots was harvested including roots.

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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 treatments (with three replicates) at the beginning of the experiment to obtain soil solution. Selected pots with installed suction cups were watered with deionized 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 content 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 grown on medium contaminated soil showing no visible symptoms of toxicity. We calculated the weighted mean of metal concentration in shoots with respect to element concentrations in particular plant structures and yields in dry weight. From these results, we compared accumulation ability of tested plant species. Both hyperaccumulators confirmed their extremely high trace element accumulation capacity compare to other tested species (Table 1). Although they never exceeded the hyperaccumulation threshold value, they were able to take up significantly higher concentrations of As, Cd, Pb, and Zn than planted trees. This was particularly observed in the case of As and Zn. In general, both hyperaccumulators took up a significantly higher trace element dose compared to other plant species. Comparing among the fast growing trees, willows accumulated usually more Cd and Zn than poplars, especially S. dasyclados. On the other hand, poplar trees took up more lead compared to willows. Concerning arsenic, no significant differences were observed among willow and poplar species.

Detailed evaluation of the data showed that only lead concentration in T. caerulescens was significantly higher than in other plant species. Concentration of Pb in A. halleri biomass did not statistically differ from concentrations of Pb in trees.

Cadmium content in T. caerulescens significantly exceeded the levels of Cd in other species including A. halleri. Concentration of Cd, which was determined in aboveground biomass of A. halleri, did not differ from S. dasyclados and S. caprea Cd concentrations but significantly exceeded S. smithiana, P. trichocarpa, and P. nigra concentrations. This corresponds

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96

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 x

Rf

Cd x

Rf

Pb x

Rf

Zn x

Rf

A. halleri T. caerulescens S. smithiana S. dasyclados S. caprea P. trichocarpa P. nigra

6.07a 5.30a 1.25b 0.964b 1.08b 0.825b 0.918b

0.067a 0.028b 0.035b 0.033b 0.038b 0.039b 0.047ab

82.3a 271b 23.6c 41.1ac 32.8ac 20.4c 17.3c

4.75abc 7.55cd 3.36a 8.10d 6.38cd 5.0abc 4.58ab

21.9a 57.6b 6.84a 10.9a 8.14a 17.3a 16.7a

0.008ab 0.010ab 0.005a 0.012b 0.008ab 0.024c 0.025c

2746a 1500b 432c 591c 475c 337c 344c

2.92a 0.963d 1.17cd 2.24ab 1.79bc 1.61bcd 1.77bc

Dmin

1.85

0.023

2.66

19.1

0.005

50.2

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 to accumulate more Cd than poplar plants. Concentrations of arsenic and zinc in both hyperaccumulators significantly exceeded concentrations of these elements in trees and no statistical differences among element concentrations in the analyzed tree species were determined. From this point of view there could be more advantageous to plant hyperaccumulators than to other plant species due to high concentration of elements in the aboveground biomass. We have determined similar concentrations of each element in shoots of trees in both years while in biomass of A. halleri the element concentrations decreased in the second vegetation period. Likewise, in leaves of T. caerulescens the Pb levels decreased while Cd and Zn levels increased in the second year (data not showed). It is partly in accordance with Keller and Hammer (2004) who concluded a significant increase in the concentration of Zn in the leaves in three following T. caerulescens croppings, but they did not register changes in the concentration of Cd in plants grown on unamended soil.

3.2. Remediation capacity Remediation technologies appoint to remove the majority of elements from contaminated soil. The total element content in aboveground biomass is only one of the factors. The most important component is probably the remediation factor (Rf), which represents percentage of element removed per year from a determined volume of soil with the respect to plant element concentration and plant yield. The calculation was already published in Vyslou zilova´ et al. (2003) or Zhao et al. (2003). In our experiment, the plant species with lower element concentration in shoots compensated the remediation effectiveness by great biomass production compared to plant species with higher element concentration and low biomass production (Table 1).

Despite statistically significant differences in calculated remediation factors there was practically no difference in remediation efficiency between hyperaccumulators and selected trees, especially for S. dasyclados. The use of these species may have a similar effect. Remediation factor of willow varied with plant genotype. Greger and Landberg (1999) concluded that some varieties of Salix spp. have a remediation capacity of about five times higher than hyperaccumulators

(T. caerulescens or Alyssum murale) due to the high biomass production and transport of Cd and Zn to shoots. Ratio of elements removed from the soil by plants proportionally decreased with increasing total content of element in soil. This is partly in accordance with our results. We registered similar or a slightly higher remediation capacity for S. dasyclados (optionally poplar trees for Pb) compared to hyperaccumulators. In contrast, Keller et al. (2003) considered T. caerulescens as a more efficient species in trace element removal than Salix viminalis or Nicotiana tabacum due to higher total element concentration in aboveground biomass. On the other hand, willow (Salix viminalis), showed a great remediation potential, as well.

Klang-Westin and Eriksson (2003) observed higher content of Cd in leaves and stems of smaller willow plants compared to much bigger yielding plants. Schwartz et al. (2003) observed the same effect in T. caerulescens shoots. Obviously there are no significant differences in Thlaspi and selected Salix species regarding remediation capability.

We investigated element shoot/root accumulation ratio to assess its transport within the plant tissue. Fig. 1 shows a good likelihood of all tested species to transport Cd and Zn from roots to aboveground biomass. All species deposit As and Pb preferentially in roots. The highest shoot/root Cd ratio was found in A. halleri, S. dasyclados, P. trichocarpa and P. nigra. Significantly higher transport of Zn was observed in both poplar species compared to other ones. This is in accordance with results of many other authors that described the highest concentration of Cd and Zn in poplar or willow leaves compared to other plant structures (Pulford 3

2

1

0 Cd

As AH

TC

SS

Pb SD

SC

Zn PT

PN

Fig. 1. Average element accumulation shoot/root ratio of different plant species (n ¼ 4).

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

and Watson, 2002). We are able to conclude that poplar trees are indeed capable of transport Cd and Zn to shoots, but their remediation factor is lower in contrast to both hyperaccumulators and S. dasyclados. From the practical point of view, it is easier to use trees because of their greater biomass production and easier treatment, harvest, and later manipulation with biomass compared to small hyperaccumulators. Tree utilization in soil remediation has more advantages than herb planting.

Trees, such as poplars, are able to transpire more water, they can get water from deeper soil horizons, and they have better regeneration capability than herbs (most of hyperaccumulator species), especially in spring revegetation (Pierzynski, 1997).

3.3. Available content of metals in soil Many authors have realized the relationship between trace element soluble concentrations in the soil and in plants (Schmidt, 2003). Available concentration of metals in the soil is usually determined using 0.01 mol L 1 CaCl2 or 1 mol L 1 NH4NO3 extraction (Hornburg and Brummer, 1993; Degryse et al., 2003; Pueyo et al., 2004). Kabata-Pendias and Pendias (2001) compared available trace element content from several soils measured in 0.01 mol L 1 CaCl2 solutions and soil solutions from porous suction cups. Extract of CaCl2 contained 21e180 mg L 1 of Zn and presence of As, Cd, and Pb was not detected. Soil solution from suction cups 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. Wenzel et al. (2002) determined 0.3e101.4 mg L 1 of As measured in soil solution according to soil type, horizon, and depth. In our experiment we determined concentration of elements in CaCl2 solution at different intervals 12.2e31.8 mg L 1 of

97

As, 6.1e72.6 mg L 1 of Cd, 200e1009 mg L 1 of Pb, and 120e1236 mg L 1 of Zn. Soil solutions extracted from the pots were used to measure metal concentrations in the range of 25.1e35.6 mg L 1 of As, 1.6e8.2 mg L 1 of Cd, 16.1e 100 mg L 1 of Pb, and 31.6e838 mg L 1 of Zn, respectively.

However, this comparison is the critical point. As it is expected, the data published in literature and element concentrations measured in this experiment are weakly comparable because of extractions and analyses provided in specific soil conditions and/or experimental parameters of individual trials.

In total six soil solution samples for each of the two vegetation periods (three suctions per year) were carried in order to determine changes in available concentration of trace elements in the soil during the vegetative growth. Furthermore, a comparison between element concentration in soil solution and element concentrations determined in traditional soil extracts (0.01 mol L 1 CaCl2 extraction) was conducted. Soil samples intended for laboratory procedure (CaCl2 extraction) were released at the end of the vegetative period. Control variant lacking plant vegetation cover was used for this determination. In most cases, element content determined in CaCl2 extraction exceeded the concentration measured in soil solution for all studied plant species (Fig. 2). Only a few exceptions did not correlate with these results. From heavy metals only Zn concentration in the control treatment did not follow this pattern.

A slightly different situation was observed for arsenic. The concentration of arsenic in CaCl2 extract overstepped (not significantly) As content in soil solution only in S. smithiana treatment. Significant differences of Cd and Pb concentrations in soil solution as well as CaCl2 extract raises concerns about applicability of CaCl2 extraction to determine available content of these elements in the soil. Moreover, significant

Arsenic

Cadmium

40 60

g L-1

g L-1

30 20

40

20

10

0

0 TC

SS

SD

SC

Soil solution

PN

control

TC

SD

SC

Soil solution

Lead

PN

control

CaCl2

Zinc 623

400

1.05

925 1.0 0.8

mg L-1

300

g L-1

SS

CaCl2

200 100

0.6 0.4 0.2

0

0.0 TC

SS

SD Soil solution

SC

PN CaCl2

control

TC

SS

SD Soil solution

SC

PN

control

CaCl2

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

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

98

differences in element extractability by individual extracting agents were documented by Hornburg et al. (1995) who determined higher content of metals in CaCl2 extract compared to NH4NO3 solution.

Kabata-Pendias and Pendias (2001) found very similar content of trace elements in soil solution from various soils and we measured more or less similar concentrations of trace elements in soil solution from different plant treatments. Changes in element available portion in soil solution of different plant species were evaluated with respect to time. Zhang et al.

(1998) described the resupply of trace elements available fractions in the soil. In our measurements we were able to record a decrease in Cd and Zn concentration compared to the control assay for most of the time during the experiment (Fig. 3, data for Zn is not shown) given by plant trace element uptake as described also by Sza´kova´ et al. (2003). Relatively constant concentration of elements in the soil solution during the vegetative growth confirms the theory of continuous element resupply. On the third suction (at the end of the first vegetation year) of the treatment with S. dasyclados we can see a sharp increase in the concentration of Cd in soil solution.

This was probably caused by lower plant element uptake with constant element resupply processes in the soil. In the second year there were no strong deviations like this one, probably due to climatic conditions (warm summer in the first year and cold weather in the second year).

Cadmium 30

g L-1

20

4. Conclusions

10

0 1

2

3

4

5

6

Suction Nr. TC

SS

SD

SC

PN

control

Lead 200

150

g L-1

At the end of both vegetative periods, the lead content in soil solution of different plant species slightly increased.

This was probably caused by a restriction in plant element uptake. All tested plant species, contained slightly higher concentrations of Pb in soil solution compared to the control treatment. Soil solution of P. nigra contained a higher Pb concentration than other species including the control treatment all the time. This was probably caused by root exudates with a wide range of organic and inorganic substances, which inevitably led to changes in soil biochemical and physical properties (Walker et al., 2003) and metal mobilization. Poplar trees are able to remediate relatively high ratio of Pb, as described above. We calculated the best remediation effectiveness for both poplar species compared to other species analyzed. Evaluation of arsenic content showed only possible decreases in the concentration of this element between the first and the second year of cropping. There are no evident trends in plant element uptake or mobilization in the soil (data not shown).

Our results showed a significant impact of plant species and its capability to take up trace elements from the soil and accumulate them in aboveground biomass. Some plant species are able to influence the available pool of elements in the soil due to root exudates and are also capable of removing trace elements compared to other species. These results come from the pot experiment. In general, plants grown in pot experiment usually contain higher concentrations of trace elements than plants grown in the field. Plants grown in the field showed a 20% decrease of remediation efficiency compared to the plants from pot experimental conditions (Schmidt, 2003). In spite of this it is necessary to understand the principles of phytoremediation and the processes that occur under regulated conditions prior to use in contaminated areas.

100

50

0 1

2

3

4

5

6

Suction Nr. TC

SS

SD

SC

PN

control

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

Widespread need to remediate soils in areas contaminated with high concentrations of trace elements generates interest about environmental friendly remediation technologies. Phytoremediation uses plants to decrease soil pollution to an acceptable level. It is necessary to find plant species with a good accumulation capacity and remediation capability.

Seven plant species with different yield and accumulation ability were tested in our experiment for their remediation characteristics. We have confirmed hyperaccumulation possibility of A. halleri and T. caerulescens for Cd and great accumulation ability for other studied elements. Very good accumulation was determined in tested trees, too. In particular, willow S. dasyclados compensated lower metal content in shoots with higher biomass production compared to hyperaccumulators, which have higher element content but lower aboveground biomass resulting in similar remediation capability.

Although poplar trees showed the best willingness to transport Cd and Zn from roots to shoots, their remediation potential does not achieve S. dasyclados or hyperaccumulators level.

Available concentrations of trace elements in soil measured in direct soil solution were observed, too. We have recorded no significant differences of element concentrations in soil

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

solution in time. Results indicate that plant character and root exudates have preferential effects on trace elements uptake and accumulation by plants.

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

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