Natural Revegetation in the Vicinity of the Former Lead Smelter in

The response of plant communities to pollution associated with the lead smelter in Zerjav, Slovenia, was investigated on spatial and temporal scales. ...
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Environ. Sci. Technol. 2006, 40, 4119-4125

Natural Revegetation in the Vicinity of the Former Lead Smelter in Zˇerjav, Slovenia TATJANA VIDIC,* NEJC JOGAN, DAMJANA DROBNE, AND BARBARA VILHAR Department of Biology, Biotechnical Faculty, University of Ljubljana, Vecˇna pot 111, SI-1001 Ljubljana, Slovenia

The response of plant communities to pollution associated with the lead smelter in Zˇ erjav, Slovenia, was investigated on spatial and temporal scales. In 2001, the total concentrations of contaminating metals in the soil measured at the most polluted plot were 59 000 mg kg-1 Pb, 180 mg kg-1 Cd, and 3300 mg kg-1 Zn. A negative correlation between the concentration of metals in the soil and plant biodiversity parameters along the gradient of pollution in 2001 was detected. Plant species lists were compiled in 2001 for plots located at different distances from the emission source and compared to that of 1981. In the period from 1981 to 2001, smelter emissions were reduced, and plant species richness increased at all examined plots. Among the successful survivals were some metal hyperaccumulators (Minuartia gerardii, Thlaspi praecox, and Biscutella laevigata). Of special interest were plants that survived the period of highest pollution. We believe that these species can be used in metal-degraded environments for natural revegetation to immobilize heavy metals. The ecosystem in the surroundings of the former smelter is presently recovering. Our results suggest that high metal concentrations in soil are a potential limiting factor for revegetation.

Introduction The smelting industry causes extensive damage to ecosystems through emissions of SO2 and long-term atmospheric deposition of metal-containing particles, resulting, among other effects, in extreme deterioration of vegetation. The toxic effects of metals and changes in the nutrient status of the soil subject the vegetation to a strong selective pressure (1). Different plant species show varying resistance to airborne and soil-accumulated toxic elements, which is reflected in their growth, survival, and occurrence along pollution gradients (2). Vegetation damage along metal pollution gradients has been reported several times (1, 3-5). Smelter emissions have severe effects on the surrounding terrestrial ecosystem, which depends on their duration and intensity. Ecosystems around smelters are usually characterized by a species-poor grassland, such as the monoculture of some grass species (6). Only a few tolerant species are dominant in the ground vegetation at the most polluted sites. Baker and Proctor (7) found that the majority of widespread British metal-tolerant taxa are representatives of only three families: Poaceae, Brassicaceae, and Caryophylaceae, while * Corresponding author phone: +386 1 423 33 88; fax: +386 1 257 33 90; e-mail: [email protected]. 10.1021/es052339x CCC: $33.50 Published on Web 05/20/2006

 2006 American Chemical Society

families such as Cyperaceae, Asteraceae, Rosaceae, and Apiacea are poorly represented. Plant communities at polluted sites usually lack coniferous trees, mosses, and lichens. Also only a few species of herbaceous shrubs and grasses are able to survive (1, 3, 4). One of the basic conditions for the colonization of metalliferous soils is the ability of a plant species to evolve metal resistance (6). The resistance is achieved either by restricting the metal uptake by the plant or by binding heavy metals in cellular compartments (8). In addition, early colonizing species also modify metalliferous soils and so facilitate the colonization of less metal-resistant plant species (6). Studies of vegetation deterioration and natural recovery on smelter-polluted sites provide valuable information for phytoremediation of such areas. Such studies are scarce (9, 10), since they demand long-term monitoring. Hyperaccumulators are plant species often recommended for phytoremediation (11), since they accumulate exceptionally large amounts of heavy metals in their tissues (12). Metal hyperaccumulating species include herbs, shrubs, and trees. Common characteristics of these plant species are their restricted field distribution and high degree of endemism (13). Phytoremediation with hyperaccumulators has appeared to be a very promising technology in the removal of heavy metal excess from soils (14). In the present study, we analyzed the response of plant communities to pollution associated with the lead smelter in Zˇ erjav (Carinthia, Slovenia). The effect of pollution on plant communities around the lead smelter in Zˇ erjav was first studied in 1981 (4). These data were compared to plant communities analyzed after 20 years. In addition, we compared plant communities among different sampling plots, located at different distances from the emission source. We identified plant species that were resistant to the cumulative effects of smelter-associated pollution and successful in colonization of the most polluted areas around the former lead smelter. Furthermore, we discuss the importance of natural revegetation of metal-contaminated sites.

Experimental Section Study Area. The study area is located near the lead smelter in Zˇ erjav, Slovenia, which is situated in a valley at 500-575 m above sea level (asl) with surrounding mountains surmounting the valley up to 900 m (15). The smelter is connected by an underground shaft to the chimney stack, which is located about 300 m away from the plant behind a low ridge (Figure 1). The smelter started operating at the present location in 1896. At the peak of lead production in the 1970s, the smelter emitted 5000 kg of particles daily, containing 2000-2500 kg of Pb (15). A filtering system installed in 1978 drastically reduced the daily emission of particles to 70 kg (15). With the progressive reduction of lead smelter output, the emissions of SO2 gradually decreased from 6000 tonnes per year in 1976 to 700 tonnes in 1991 (16). In 1990, the primary lead smelter was converted to an industrial facility for recycling lead batteries. Annual emissions of particles ranged from 6500 to 1500 kg, and annual emissions of SO2 were about 700 tonnes. In the 1920s, the forest (Fraxino-Pinetum Martin Bosse and Ostryo-Fagetum M. Wraber ex Trinajstic´) still occurred on the slopes around the smelter (4, 17), but through decades of pollution it was gradually replaced by severely eroded grassland, with barren rocks and scree on the slopes closest to the chimney. The extent of vegetation damage caused by the smelter is reflected in the official geographical name of the affected area, Dolina smrti (The Death Valley). VOL. 40, NO. 13, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Aerial photograph of the valley of Dolina smrti in 1997: Sm, lead smelter in the village of Zˇ erjav; Ch, smelter chimney. (Note that the smelter is connected to the stack with an underground shaft, dotted line.) Numbers denote sampling plots on the central ridge: 0 (distance from chimney 100 m), 2 (150 m), 3 (200 m), 4 (260 m), 5 (330 m), 6 (420 m), 7 (520 m), 8 (670 m). Plot R (located in an adjacent valley to the east, distance from the chimney approximately 2 km) is not shown on the photograph. Reprinted with permission. Copyright 2006 Geodetska uprava Republike Slovenije. The plants occurring in the valley were and to a large extent still are exposed to multiple stress factors: emissions of SO2 and metal-containing particles, extremely high concentrations of metals (Pb, Cd, and Zn) in the soil, drought, erosion by water, and occasional fires. Investigated Plots. Eight sampling plots were selected on the central ridge in Dolina smrti (Figure 1), at different distances from the smeltery stack: plot 0 (100 m from the stack, 690 m asl), plot 2 (150 m, 710 m asl), plot 3 (200 m, 730 m asl), plot 4 (260 m, 760 m asl), plot 5 (330 m, 800 m asl), plot 6 (420 m, 825 m asl), plot 7 (520 m, 865 m asl), plot 8 (670 m, 875 m asl). Plots 5-8 coincided with plots 2, 4, 6, and 9 analyzed in the study of Drusˇkovicˇ in 1981 (4). A reference plot R was located in an adjacent valley (about 2 km away from the stack, 700 m asl) and was not directly exposed to smelter emissions. The plots were similar in terms of the parent material, exposition, and inclination, except where geomorphology of the central ridge prevented the selection of completely comparable sites. Plots 2, 3, and 4 were steeper than other plots. Plot 0 was different from all others by being situated on a rocky outcrop immediately above the chimney. The size of all plots was 10 m × 10 m. Analysis of Soil Samples. At each plot, soil was collected on March 30, 2002, at eight evenly spaced points, mixed together, dried, and sieved to 0.05, one-way analysis of variation with Tukey-Kramer’s post test) are marked with the same label in superscript. Detection limits: Pb (20 mg/L), Cd (1.5 mg/L), and Zn (1.0 mg/L).

a

pHs

129f (1) 0.43b (0.01) 554b (18) 16.6g (0.2) 1395c (69) 22.3c (1.0) 2282e (99) 87.2e (1.0) 1276c (7) 1.80b (0.02) total AA Zn

517b (29) 1.68b (0.04)

1320c (12) 27.6c (0.1)

3273d (41) 163.9d (2.6)

2441e (92) 94.7f (1.5)

1.03b (0.04) 0.47b (0.01) 37.7h (0.0) 6.25h (0.05) 77.6g (0.0) 9.4d (0.1) 138.3f (3.6) 27.0g (0.4) 120.0e (1.1) 19.7f (0.1) 184.3d (0.8) 41.4e (0.3) 60.5c (0.3) 9.6d (0.1) 56.0c (0.2) 3.70c (0.02) total AA Cd

4.6b (0.1) 1.29b (0.03)

115b (2) 3.0b (0.1)

R 8

6976h (82) 292c (3) 15 217c (163) 794g (20)

7 6

20 133g (490) 819g (1)

5

33 320f (706) 2062f (10)

4

59 290e (1167) 4447e (90) 10 807d (257) 594d (4)

3 2

13 747c (133) 247c (1) 455b (16) 16.0b (0.5)

0 plot

total AA Pb

TABLE 1. Concentrations of Metals (Pb, Cd, and Zn) in the Soil (mg/kg Dry Soil) in 2001a

FIGURE 2. Concentration of metals in the soil and diversity indices at plots 0-8 in 2001. Data for metal concentrations were normalized so that for each metal the highest detected concentration corresponded to the value of 1 (a.u., arbitrary units; see Table 1 for absolute concentrations of metals). occurring at different plots were compared with an analysis of six Ellenberg indices (22). The Ellenberg indices at the investigated plots were similar, with median values of 7 for index L (light) at all plots and in the range 3-5 for T (temperature), 4-5 for K (continentality) and F (moisture), 7-8 for R (soil pH), and 2-3.5 for S (soil nitrogen), showing that the general ecological conditions were comparable at all plots. To examine the relationship between the total concentrations of Pb, Cd, and Zn in the soil and biodiversity, the curves showing Shannon’s diversity index and species evenness were superimposed over the graphs for total metal concentrations (Figures 2a and 2b). The peak of metal concentrations at plot 4 coincided with the lowest values of both biodiversity indices. High values of both biodiversity indices were recorded at plots less contaminated with metals (Figures 2a and 2b). Shannon’s diversity index showed a very similar spatial pattern to the species evenness (Figures 2a and 2b). The highest values of both diversity indices were recorded for unpolluted plot R (data not shown). The data indicated a negative association between metal concentrations in the soil and the diversity indices except for plot 0. At this plot soil contamination with metals (Pb, Cd, and Zn) was the lowest among all plots located on the central ridge VOL. 40, NO. 13, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 3. Comparison of vegetation parameters on the central ridge in 1981 and in 2001. The number of plant species at plot R, located in an adjacent valley approximately 2 km away from the chimney, is not shown (106 species). Data for 1981 were obtained from Drusˇ kovicˇ (4). of the valley (Table 1); however, the diversity indices were not the highest. Plot 0 was located the closest to the smelter chimney, on a rocky outcrop, where the soil was much eroded by water. The correlation between the total concentrations of contaminating metals in the soil and biodiversity parameters 4122

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(Shannon’s diversity index and species evenness) was marginally nonsignificant, with the p-value slightly above 0.05 (Table 2 in the Supporting Information), indicating a negative association between the total concentration of metals in the soil and the biodiversity. However, the correlation between the concentration of metals extracted

by ammonium acetate and Shannon’s diversity index and species evenness was significant in all cases (Table 2). In Dolina smrti, species richness was the lowest at plot 4 with only 14 species from 8 families and the highest at plots 7 and 8 with 44 species from 21 families and 42 species from 26 families, respectively (Figures 3b and 3c). Plot R showed a considerably higher species richness than the plots in Dolina smrti, with 106 plant species from 40 families (Figure 3c). In total, 78 plant species were recorded on the central ridge. The dominant plants were perennial grasses (5 species) and herbaceous dicot perennials (47 species; Table 3 in the Supporting Information). Some shrubs and a few trees were also observed, but the size of these woody plants was smaller than would be expected for adult specimens of the respective species under similar climatic conditions. Plant species that occurred in more than sporadic abundance at the most polluted plot 4 were two grasses (Sesleria varia and Calamagrostis varia), three species from the family Caryophyllaceae (Minuartia gerardii, Silene alpestris, and Silene pusilla), and one species from the family Brassicaceae (Thlaspi praecox; Table 3). These three families were dominant also at plots 5 and 6. Comparison of plant communities occurring at different plots with cluster analysis showed that the unpolluted plot R had a different species composition than plots 0-8 located in Dolina smrti (Figure 4 in the Supporting Information), indicating that the polluted sites were characterized by specific vegetation. Plots with similar metal concentrations in the soil had similar species compositions (plots 2 and 3, plots 5 and 6, plots 7 and 8) (Table 1, Figure 4). Plot 0, which had low metal concentrations in the soil but was located closest to the chimney, had vegetation relatively different to other plots. Plot 4 as the most polluted site occurred in the group of plots 2-6 as a separate subgroup (Figure 4). Vegetation Changes in the Period 1981-2001. For four of the eight plots in Dolina smrti investigated in 2001 (plots 5-8), plant species lists were also recorded in 1981 (4), allowing for comparison of vegetation in the period of extreme pollution (1981) and after the smelter emissions were reduced (2001). At all four plots, ground cover, plant species richness, and family richness were higher in 2001 than in 1981 (Figures 3a-c). Furthermore, Shannon’s diversity index and species evenness increased at plots 6-8 in the period 1981-2001 (Figures 3d and 3e). However, plot 5 showed a decrease of these two indices (Figures 3d and 3e), although the number of plant species increased from 14 to 20 (Figure 3b). In 1981, the ground cover at plot 5 was only 25% (Figure 3a), with several species occurring at a comparably low abundance (Table 3). The improvement in the total ground cover to 85% in 2001 was largely due to spreading of Sesleria varia, resulting in an increase in its total abundance, calculated on the basis of ground cover, from 7 to 50% (Figure 5a in the Supporting Information) and its relative abundance in the plant community from 30 to 60%. In general, changes of the biodiversity parameters in the period 1981-2001 showed that the vegetation in Dolina smrti has recovered during the last 20 years. The status of plant species recorded at plots 5-8 in 1981 and in 2001 is shown in Figure 3f, where species were classified either as survivors (present in 1981 and 2001), newcomers (absent in 1981, present in 2001), or disappearers (present in 1981, absent in 2001). All plots showed considerable changes in species composition during the last 20 years. Plots 5 and 6 had a similar class composition (Figure 3f). Plot 7 showed the most pronounced changes between 1981 and 2001, with 60% of newcomers, compared to 40% at the least polluted plot 8 (Figure 3f). The number of survivors was the highest at plot 8. Nevertheless, the number of newcomers was higher than the number of disappearers at these four

plots, and the total number of species recorded at plots 5-8 was 51 in 1981 and 69 in 2001. In the period from 1981 to 2001 changes in plant communities were investigated for plots 5-8. In 1981, the species composition at the least polluted plot 8 was different from the cluster of plots 5, 6, and 7 (Figure 4 in the Supporting Information). Vegetation at plots 5, 6, and 7 in 1981 was relatively dissimilar to vegetation at the respective plots in 2001, indicating relatively large changes due to natural vegetation recovery. In this period, plots 5 and 6 experienced similar changes in vegetation composition, appearing together as a separate subgroup in 2001, and vegetation at plot 7 became similar to the least polluted plot 8 (Figure 4).

Discussion The evidence presented in this study demonstrates that vegetation in Dolina smrti has recovered to some extent in the period 1981-2001, presumably due to reduced emissions from the smelter in the 1980s and in particular in the 1990s, when the primary lead smelter was converted to an industrial facility for recycling lead batteries. However, biodiversity was still relatively low at some of the most polluted plots in 2001. At some plots in Dolina smrti, the total concentrations of Pb, Cd, and Zn in the soil were extremely high (Table 1). The source of these metals could be either the parent material or atmospheric deposition of metal-containing particles. The parent material at our sampling plots is noric dolomite and does not contain elevated amounts of Pb, Cd, and Zn. Distribution of the total concentrations of Pb, Cd, and Zn in the soils from plots 4-8 decreased with increasing distance from the smelter chimney (Figure 2), which is in agreement with previous reports (3, 27-30). Lower concentrations of metals in the soil at plots 0-3, located closest to the smelter chimney, could be due to plume rise under normal atmospheric conditions. Our observations support the conclusion that in Dolina smrti the major source of Pb, Cd, and Zn in the soil is the long-term deposition of metal-containing particles emitted from the smelter chimney. Around large smelters, the area of damaged vegetation extends many kilometers away from the source of emissions (1, 3, 10). In Dolina smrti, plants experience an extreme gradient of pollution over a few hundred meters, and the valley is thus a unique small field laboratory for studies of the impact of smelter-associated pollution on the ecosystem. In particular, no barrier exists for spreading of the seeds over the short distance from the edges of the valley to the central ridge. Hence, the differential species composition on the investigated plots can be attributed to stress factors associated with pollution. We observed a gradient of plant diversity on the central ridge in Dolina smrti in 2001 associated with the level of extractable metal fraction (Table 2 in the Supporting Information). The concentration of metals extracted by ammonium acetate could be regarded as a better estimate of metal phytoavailability than the total metal concentration (18, 31). The significant negative correlation between vegetation parameters and concentrations of extractable Pb, Cd, and Zn in the soil (Table 2 in the Supporting Information) indicates that at present elevated concentrations of metals in the soil are potentially still a major factor limiting vegetation recovery. A similar gradient in plant diversity existed also in 1981 (4). A decrease of plant species richness caused by smelterassociated pollution has been described before for different types of smelters, for example, for the Morchegorsk nickel smelter (3), the Ventanas copper smelter (32), and the copper-nickel smelter at Harjavalta (1). Salemaa et al. (1) also reported a negative correlation between the distance from the smelter and Shannon’s diversity index and species evenness. While the data for plots 4-8 are consistent in showing that metal concentration in the soil decreases and VOL. 40, NO. 13, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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biodiversity increases with increasing distance from the emission source (Figure 2), it is difficult to adequately interpret the data for plots 0-3. These plots were located very close to the chimney, but the total metal concentration in the soil indicates that they may be less exposed to longterm deposition of particles. It is possible that these plots experienced high short-term concentrations of emissions, in particular SO2, at specific atmospheric conditions, such as temperature inversion reported to occur frequently in the valley (15). Furthermore, we believe that the natural recolonization at plot 0 was probably limited by severe loss of soil through erosion by water. Several plant species occurring at plots with the highest concentrations of Pb, Cd, and Zn in the soil have been described before as metal hyperaccumulators: Minuartia gerardii (syn. M. verna p.p.; ref 17), Thlaspi praecox (13, 33), and Biscutella laevigata (18). Notably, all three species were spreading in the valley during the last 20 years and were recorded at all plots in Dolina smrti in 2001 (Table 3 and Figure 5 in the Supporting Information). In 1981, Minuartia gerardii and Thlaspi praecox were recorded only at plot 8, while Biscutella laevigata occurred at plots 6 and 7 (Table 3, Figure 5). A possible explanation for this is that these plants can survive at high metal concentrations in the soil, but they may be relatively sensitive to SO2 or to foliar deposition of metal particles. It is possible that these plants invaded the valley only after emissions of SO2 or foliar deposition of metal particles were reduced. Drusˇkovicˇ (34) also reported that plants on the central ridge showed a reduced seed production when compared to those from unpolluted sites and were propagating mainly vegetatively. Wierzbicka and Obidzin ´ ska (35) detected a smaller seed size and lower germinability in calamine populations of several plant species, including Biscutella laevigata, compared to populations from normal soils. Reproductive incompetence caused by pollution may thus be a factor limiting the establishment of new species on the central ridge in Dolina smrti. The improvement of vegetation in the period 1981-2001 suggests that before 1981 factors other than phytoavailable metals in the soil represented important limitations for establishment of plant species. Most likely these included high concentrations of SO2 (2, 4) and foliar deposition of metal-containing particles (36). Plant species recorded on at least three of the four investigated plots 6-8 both in 1981 and in 2001 were Acinos alpinus, Erica carnea, Erysimum sylvestre, Sesleria varia, and Solidago virgaurea (Table 3). Among these species, Sesleria varia was the most important ground-covering plant, showing a stable high abundance in the period 1981-2001 (Figure 5a in the Supporting Information). For example, the improvement in ground cover at plot 5 from 25% in 1981 to 85% in 2001 (Figure 3a) was largely due to the spreading of Sesleria varia (Figure 5a). The spatial distribution of Sesleria varia shows that this species was the most abundant at plots with the highest concentrations of contaminating metals in the soil, indicating its resistance to metal pollution. Among woody plants, Salix caprea and S. glabra were the most abundant (Table 3 in the Supporting Information), but woody species were in general underrepresented in the vegetation of the central ridge in Dolina smrti. Natural vegetation recovery due to reduced emissions from the smelter is a specific phenomenon related to metal pollution. Previous to our investigation, natural revegetation around smelters has been assessed with studies of aerophotographs (10) and with descriptive analysis of vegetation (9). The present study presents evaluation of natural vegetation recovery on smelter-polluted soil, based on comparative analysis of species composition and abundance at specific plots in the period of severe pollution and after emissions were reduced. Our results demonstrate that in the period of 4124

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reduced emissions the ecosystem is in a dynamic state of succession. Plant species richness increased when the emissions were reduced, but not only due to new arrivals, but also due to survivors, which spread from distant plots to plots located closest to the smelter chimney. Some species disappeared at specific plots in the period from 1981 to 2001, and some of the surviving species increased in abundance (Table 3). Notably, several metal hyperaccumulating species were among the successful survivors. Our preliminary results showed that Thlaspi praecox hyperaccumulated Cd, while Minuartia gerardii hyperaccumulated Pb. The limiting value for hyperaccumulation of Zn was not exceeded in either of the two examined species (37). We presume that some other species on the list (Table 3) are potential candidates for having metal remediation capabilities. We believe that plants surviving the period of highest pollution can be used in most metal-degraded environments for natural revegetation.

Acknowledgments We thank Dr. Blanka Drusˇkovicˇ for helping us to identify the plots of the 1981 study and for valuable information and Bozˇo Frajman, Tinka Bacˇicˇ, and Iztok Tomazˇicˇ for help with field work.

Supporting Information Available Species composition and abundance on the central ridge, dendrogram showing similarity in species composition among plots in Dolina smrti, and correlation between concentration of metals in the soil and biodiversity parameters. This material is available free of charge via the Internet at http://pubs.acs.org.

Literature Cited (1) Salemaa, M.; Vanha-Majamaa, I.; Derome, J. Understorey vegetation along a heavy-metal pollution gradient in SW Finland. Environ. Pollut. 2001, 112, 339-350. (2) Salemaa, M.; Derome, J.; Helmisaari, H. S.; Nieminen T.; VanhaMajamaa, I. Element accumulation in boreal bryophytes, lichens and vascular plants exposed to heavy metal and sulfur deposition in Finland. Sci. Total Environ. 2004, 324, 141-160. (3) Chernenkova, T. V.; Kuperman, R. G. Changes in the spruce forest communities along a heavy metal deposition gradient on Kola Peninsula. Water, Air, Soil Pollut. 1999, 111, 187-200. (4) Drusˇkovicˇ, B. Spremembe rastlinskih populacij v okolici topilnice svinca. Biol. Vestn. 1985, 33, 23-38. (5) Vike, E. Air-pollutant dispersal patterns and vegetation damage in the vicinity of three aluminium smelters in Norway. Sci. Total Environ. 1999, 236, 75-90. (6) Ernst, W. H. O. Mine vegetation in Europe. In Heavy Metal Tolerance in Plants: Evolutionary Aspects; Shaw, A. J., Ed.; CRC Press: Boca Raton, FL, 1990. (7) Baker, A. J. M.; Proctor, J. The influence of cadmium, copper, lead, and zinc on the distribution and evolution of metallophytes in the British Isles. Plant Syst. Evol. 1990, 173, 91-108. (8) Baker, A. J. M. Metal tolerance. New Phytol. 1987, 106, 93-111. (9) Gunn, J.; Keller, W.; Negusanti, J.; Potvin, R.; Beckett, P.; Winterhalder, K. Ecosystem recovery after emission reductions; Sudbury, Canada. Water, Air, Soil Pollut. 1995, 85, 1783-1788. (10) McCall, J.; Gunn, J.; Struik, H. Photo interpretive study of recovery of damaged lands near the metal smelters of Sudbury, Canada. Water, Air, Soil Pollut. 1995, 85, 847-852. (11) Ernst, W. H. O. Phytoextraction of mine wastessOptions and impossibilities. Chem. Erde 2005, 65, 29-42. (12) Wierzbicka, M.; Pielichowska, M. Adaptation of Biscutella laevigata L., a metal hyperaccumulator, to growth on a zinclead waste heap in southern Poland I: Differences between waste-heap and mountain populations. Chemosphere 2004, 54 1663-1674. (13) Baker, A. J. M.; Brooks, R. R. Terrestrial higher plants which hyperaccumulate metallic elementssA review of their distribution, ecology and phytochemistry. Biorecovery 1989, 1, 81-126. (14) Gardea-Torresdey, J. L.; Peralta-Videa, J. R.; de la Rosa, G.; Parsons, J. P. Phytoremediation of heavy metals and study of

(15)

(16) (17)

(18)

(19)

(20)

(21) (22)

(23) (24)

(25)

(26)

the metal coordination by X-ray absorption spectroscopy. Coord. Chem. Rev. 2005, 249 (17-18), 1797-1810. Fugasˇ, M.; Hrsˇak, J.; Souvent, P. The effect of a new emission control system on lead, zinc and cadmium concentrations in the environment of a lead smeltery. Staub-Reinhalt. Luft 1984, 6, 273-275. Souvent, P. Svinec, metalurgija svinca, okolje. Rud.-Metal. Vestn. 1992, 39, 447-469. Wraber, M. Tipolosˇka Razcˇlenitev Gozdne Vegetacije v Gornji Mezˇisˇki Dolini; Research Report; Porocˇila Slovenske Akademije Znanosti in Umetnosti: Ljubljana, Slovenia, 1959. Wenzel, W. W.; Jockwer, F. Accumulation of heavy metals in plants grown on mineralised soils of the Austrian Alps. Environ. Pollut. 1999, 104, 145-155. Baker, A. J. M.; Reeves, R. D.; Hajar, A. S. M. Heavy metal accumulation and tolerance in British populations of Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol. 1994, 127, 61-68. Martincˇicˇ, A.; Wraber, T.; Jogan, N.; Ravnik, V.; Podobnik, A.; Turk, B.; Vresˇ, B. Mala flora SlovenijesKljucˇ za Dolocˇanje Praprotnic in Semenk; Tehnisˇka zalozˇba Slovenije: Ljubljana, Slovenia, 1999. Braun-Blanquet, J. Pflanzensoziologie: Grundzu ¨ ge der Vegetationskunde; Springer-Verlag: Vienna, Austria, 1964. Ellenberg, H.; Weber, H. E.; Du ¨ ll, R.; Wirth, V.; Werner, W.; Paulissen, D. Zeigerwerte von Pflanzen in Mitteleuropa. Scr. Geobot. 1992, 18, 1-258. Pielou, E. C. The measurement of diversity in different types of biological collections. J. Theor. Biol. 1996, 13, 131-144. Uredba o mejnih, opozorilnih in kriticˇnih imisijskih vrednostih nevarnih snovi v tleh. Uradni list Republike Slovenije. Off. Gaz. RS 1996, 68, 5773-5774. Metals concentrations typically found in unpolluted soil and soil clean up standards. http://www.newhallinfo.org/ PDFs4download/contamination_page_docs/ metalscomparison3.pdf. Jogan, N.; Kaligaricˇ, M.; Leskovar, I.; Selisˇkar, A.; Dobravec, J. In Habitatni tipi Slovenije HTS 2004; Leskovar, I., Dobravec, J.; Eds; Agencija Republike Slovenije za Okolje: Ljubljana, Slovenia, 2004.

(27) Rieuwerts, J.; Farago, M. Heavy metal pollution in the vicinity of a secondary lead smelter in the Czech Republic. Appl. Geochem. 1996, 11, 17-23. (28) Koptsik, G. N.; Nedbaev, N. P.; Koptsik, S. V.; Pavlyuk, I. N. Heavy metal pollution of forest soils by atmospheric emissions from Pechenganikel smelter. Eurasian Soil Sci. 1998, 31, 896903. (29) Palacios, H.; Iribarren, I.; Olalla, M. J.; Cala, V. Lead poisoning of horses in the vicinity of a battery recycling plant. Sci. Total Environ. 2002, 290, 81-89. (30) Liu, Z. P. Lead poisoning combined with cadmium in sheep and horses in the vicinity of non-ferrous metal smelters. Sci. Total Environ. 2003, 309, 117-126. (31) Ernst, W. H. O. Bioavailability of heavy metals and decontamination of soils by plants. Appl. Geochem. 1996, 11, 163-167. (32) Ginocchio, R. Effects of a copper smelter on a grassland community in the Puchuncavı´ Valley, Chile. Chemosphere 2000, 41, 15-23. (33) Vogel-Mikusˇ, K.; Drobne, D.; Regvar, M. Zn, Cd and Pb accumulation and arbuscular mycorrhizal colonisation of pennycress Thlaspi praecox Wulf. (Brassicaceae) from the vicinity of a lead mine and smelter in Slovenia. Environ. Pollut. 2005, 133, 233-242. (34) Drusˇkovicˇ B. Uticaj Zagadjenja Sredine na Genetske Promene u Biljnim Populacijama. Ph.D. Thesis, University of Novi Sad, Yugoslavia, 1984. (35) Wierzbicka, M.; Obidzin ˜ ska, J. The effect of lead on seed imbibition and germination in different plant species. Plant Sci. 1998, 137, 155-171. (36) Gawel, J. E.; Trick, C. G.; Morel, F. M. M. Phytochelatins are bioindicators of atmospheric metal exposure via direct foliar uptake in trees near Sudbury, Ontario Canada. Environ. Sci. Technol. 2001, 35, 2108-2113. (37) Razinger, J. Accumulation of Pb, Cd and Zn in Tissues of Three Plant Species from the Valley Dolina smrti. Graduation Thesis, University of Ljubljana, Ljubljana, Slovenia, 2003.

Received for review November 19, 2005. Revised manuscript received March 6, 2006. Accepted March 13, 2006. ES052339X

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