Specific Metallophytes and Their Potential Role in Phytoremediation

A botanist can immediately recognize that a site has a heavy metal soil due to the occurrence of metallophytes. In Central Europe, 3-6 plant species typically occur at every site polluted with heavy metals. However, for some unknown reason, no heavy metal soil contains every metallophyte. In many cases, metallophytes are relicts from the glacial period, only occurring in the plain at sites polluted with heavy metals, but thriving in alpine regions above the timberline or close to arctic areas too. This is the case for Minuartia (= Alsine) verna, which can endure the highest concentrations of heavy metals of any Central European metallophyte. The mechanism used by this plant to cope with such high concentrations of heavy metals is not yet clear. It is said that the leaves of M. verna die when they are overloaded with heavy metals and that the plant frequently generates new leaves from the vegetation point. Armeria maritima ssp halleri also occurs in coastal salt marshes (ssp. maritima) and has a closely related species (Armeria maritima ssp. alpina) that grows in the Alps. It possesses specific glands (modified stomata) that serve to excrete toxic heavy metals taken up accidentally. Armeria maritima ssp. halleri contains 20-fold and 88-fold greater concentrations, respectively, of Pb and Cu in its roots than in its leaves, indicating that the metals are immobilized in its roots. On the other hand, high levels of Zn, Cd, Pb, and Cu in brown leaves suggest a leaf fall detoxification mechanism (Dahmani-Muller et al. 2000). The genus Thlaspi comprises several closely related species that thrive on heavy metal soils: Thlaspi calaminare in the plain; Thlaspi goesingense in a few places in Austria and in Eastern European countries (Fig. 5.2); and Thlaspi praecox and T. caerulescens in heavy metal soils as well as unpolluted sites. These members of the Thlaspi montanum-alpestre group should be differentiated from Thlaspi cepaeifolium (= T. rotundifolium ssp. cepaeifolium), which is next related to Thlapsi rotundifolium, found in alpine chalk gravel. T. cepaeifolium is highly endangered and currently only occurs at two sites polluted with heavy metals: Cave de Predil in Friaul in Northeastern Italy, and along the river bed of the Gailitz, close to Arnoldstein in Southern Austria. Since its gene pool (particularly the genes encoding heavy metal tolerance related proteins) may be significantly different from those of other metallophytes of the genus Thlaspi, T. cepaeifolium needs to be preserved by any means. Thlaspi species are generally short-living annual plants and they have developed means to keep their seeds free of toxic heavy metal concentrations. Another Brassicaceae member that occurs in almost all heavy metal soils in Central Europe (but not in the Aachen-Liège area) is Cardaminopsis (= Arabidopis) halleri. Since it is related to the model plant Arabidopsis thaliana, this plant is currently used in studies of heavy metal tolerance at the molecular level.

Zinc violets are particularly beautiful metallophytes (Fig. 5.3). Two different subspecies exist with very restricted and thus endemic occurrences. The yellow zinc violet (Viola lutea ssp. calaminaria) occupies heavy metal heaps only in the area between Aachen in Germany and Liège in Belgium, but such stands can contain thousands of these plants. The yellow zinc violet produces plenty of its striking flowers from the middle of May until about the end of September, which makes

Fig. 5.2 Thlaspi goesingense thrives on heavy metal heaps, particularly serpentine soils in Austria and Hungary. Due to its fairly high productivity, it is attractive for phytoremediation purposes

these sites worth visiting during this time. The blue zinc violet (Viola lutea ssp. westfalica) can only be seen in the lead ditch and its surrounding heaps at Blankenrode near Paderborn in Germany, where it covers an area of about 0.5 x 1 km2. Recent molecular analyzes of its DNA have indicated that both of these zinc violets stem from the alpine Viola lutea and not from V. tricolor and so should be regarded as subspecies or varieties (Hildebrandt et al. 2006a). Both occur only on heavy metal soils but can also be successfully grown in unpolluted garden soils. They are therefore not obligate metallophytes or heavy metal resistant, as claimed earlier (Nauenburg 1986). Their parents currently occur (abundantly) in alpine areas such as the Vosges mountains in France in both blue and yellow forms, rarely in the Alps, in Southern England, and also in the Carpathian and Sudeten mountains (possibly as an individual subspecies there, V. lutea ssp. sudetica). V. lutea may have had a broad distribution following the end of the last glacial period. Afterwards

Fig. 5.3 Zinc violets are beauties on heavy metal heaps. They exist in two forms: Viola lutea ssp. westfalica (the blue form), which is only found on the lead heap in Blankenrode, Eastern Westfalia, and Viola lutea ssp. calaminaria, (the yellow form) which grows on Zn-rich soils between Aachen in Germany and Liège in Belgium

Fig. 5.3 Zinc violets are beauties on heavy metal heaps. They exist in two forms: Viola lutea ssp. westfalica (the blue form), which is only found on the lead heap in Blankenrode, Eastern Westfalia, and Viola lutea ssp. calaminaria, (the yellow form) which grows on Zn-rich soils between Aachen in Germany and Liège in Belgium it may have wiped out in unpolluted sites by better-growing plants. It could therefore only survive at heavy metal sites, where it developed into the blue zinc violet of Blankenrode and the yellow zinc violet of Aachen-Liège due to their isolation. Alternatively, they may have been transported by medieval miners to heavy metal sites, where they subsequently developed into separate entities.

Zinc violets are unable to radiate to eastern or southern areas for some unknown reason. Heavy metal sites in these regions are occupied by V. tricolor, which also fascinates due to its thousands of blossoms at (for example) Boleslaw heap, close to Olkusz in Southern Poland. However, V. tricolor can also be found at unpolluted sites. It is not yet clear whether a special ecotype of V. tricolor thrives on heavy metal soils, for example in Southern Poland, on the German Harz mountains, or in Southern Austria (Bad Bleiberg). V. tricolor is also reported to occur in the western part of Germany and in Belgium, although only with a low abundance. It is somewhat surprising that V. tricolor could not conquer Western European heavy metal soils, where it is replaced by zinc violets.

Other metallophytes exist in Central Europe. Shoots of Silene vulgaris grow curved on heavy metal heaps but straight on unpolluted sites. This specific ecotype of this member of Caryophyllaceae is often regarded as a subspecies or variety (var. humilis) with an enhanced tolerance to heavy metals (Wierzbicka and Panufnik 1998). Festuca ovina may have developed a specific ecotype on heavy metal soils (Patzke and Brown 1990). However, the Festuca ovina group is difficult to resolve taxonomically. Alyssum wulfenianum is another beauty of the alpine heavy metal soils but is now almost extinct. The need to preserve such extremely rare plants for future generations must be stressed. Sites polluted with heavy metals in South Poland possess specifically adapted ecotypes of Biscutella laevigata (Wierzbicka and Pielichowska 2004) and Dianthus carthusianorum (Zalecka and Wierzbicka 2002), although these have no apparent morphological differences from the individuals thriving on uncontaminated soils. Examinations of other plants that grow on unpolluted soils as well as at heavy metal sites with almost unimpaired growth rates may provide new insights into their metal exclusion strategies. Other metallophytes have also been reported around the world (Prasad and de Oliveira-Freitas 1999). Heavy metal accumulating plants occur in diverse families and genera of the plant kingdom. Thus, metal tolerance is a typical example of convergence within plant taxonomy.

In a recent review (Ernst et al. 2008), the degree of tolerance of heavy metals was divided into three categories: hypotolerance, basal tolerance, and hypertoler-ance. Plant species do differ in their abilities to endure heavy metal stress. Tolerance even appears to vary with the heavy metal, and from one plant species to the next. Therefore, the separation into strict categories does not seem to afford us much help when attempting to explain the physiological phenomena.

All metallophytes can be grown on unpolluted soils. Probably due to the better nutrient supply present in such soils, their productivity is even higher in garden soils than at polluted sites. This was tested for several Central European metallophytes (unpublished culture data obtained from 2000 to 2003 with Viola lutea ssp. calami-naria, Thlaspi goesingense, T. calaminare, T. praecox, Armeria maritima ssp. halleri in the garden of the Botanical Institute of Cologne, and with V. lutea ssp. westfalica in a private allotment at Erftstadt, Germany). Thus, there is currently no known absolute metallophyte. The inability of metallophytes to compete with other plants might restrict their occurrence to heavy metal sites and explain their failure to radiate.

Plants that thrive on heavy metal rich soils can be used in the phytoremediation of polluted areas or postflotation wastes that are created as a by-product of ore processing. After their exploitation by mining, heavy metal soils are often a harsh substratum devoid of vegetation cover (Fig. 5.4) that make any biological reclamation difficult (Turnau et al. 2006a; Turnau et al. 2006b; Strzyszcz 2003) due to their

Fig. 5.4 Heavy metal polluted sites often have no vegetation, which causes severe problems in phytoremediation projects. Photo was taken in Kalenberg, close to Mechernich, in the Eifel mountains of Germany. Further details on this site are provided in Kaldorf et al. (1999)

toxicity, problems with slope stabilization, and drought. The dust originating from the waste heap area often contains high levels of Zn, Pb, and Cd, which pose serious health hazards for plants and animals. Typical remediation practices involve covering the waste with a layer of soil or humus, transported mostly from another area, to prevent erosion. This is followed by the introduction of trees and grasses such as Lolium perenne. Metallophytes could be used to stabilize the soils against the erosion of the surface soil by wind and rainfall, and they can colonize such disturbed areas. However, grasses, which often develop abundant root systems, were found to be more successful at phytostabilization than metallophytes. Trees such as Pinus sylvestris, Populus spp., Betula spp. and shrubs such as Hippophaë rhamnoides are also often introduced in such areas. However, in regions where fires can be expected, trees do not recover as easily as grasses. Newly established vegetation in such an area must be watered, especially if the area is steep and erosion is taking place. In order to improve the nutrient status of the wastes, experiments concerning the use of fertilizers have been carried out (Turnau et al. 2006a, b; 2008; Ryszka and Turnau 2007). If the area is relatively flat, this can be a relatively fast way of introducing vegetation; however, the compositions of such plant communities are mostly poor, and symbiotic organisms are often poorly developed.

Sustainable remedial techniques are required for such sites. Employing the remaining pre-adapted metallophyte flora seems an especially promising approach. However, there are several obstacles to the use of this technique. In a recent phyto-stabilization approach, for example, the remaining vegetation around the lead mine and smelter in Northern Slovenia was screened in order to select the most suitable plant species for further phytostabilization efforts. However, the selected dominant grass species Sesleria caerulea and Calamagrostis varia at the site did not produce enough viable offspring (Regvar et al. 2006).

Metallophytes can also be used to extract heavy metals. A specific application can be envisaged in the Chernobyl area. Radionuclides can be excavated from soils and enriched in plants. The major isotopes of Chernobyl, however, behave differently in plants. Like Ca, 90 Sr is immobile in plants and is deposited mainly in the cell walls of the roots. 137Rb, similar to K, is highly mobile in plants and can be collected in their aboveground parts. The idea is to extract radionuclides from the soils using plants and then to remove the plants to a site where the radionuclides could be concentrated.

Plants can be used for the enrichment of metals that occur in small amounts in soils; such plants are termed hyperaccumulators. Plants with the ability to accumulate high amounts of Cd, Co, Cu, Mn, Ni, and Zn include several ferns, such as Pteris vittata (Ma et al. 2001), and herbs (Ernst 2005). The use of such plants is not economically feasible for the enrichment of many elements. Most hyperaccumulators produce little aboveground biomass, they usually only accumulate particular metals, and they are not tolerant of other metals that may occur in such places. Neither hybridization of poorly productive hyperaccumulators with highly productive non-hyperaccumulators (Brewer et al. 1999) nor the use of genetically modified plants (Bennett et al. 2003, Ernst 2005) resulted in the production of lines that are significantly more effective. In terms of single elements, the use of the hyperaccumulating species Alyssum murale

(Ernst 2005), Alyssum bertelonii (Boominathan et al. 2004), Berkheya codii (Robinson et al. 2003), or of several endemic species of the serpentine flora in Zimbabwe was suggested for the enrichment of Ni (Brooks and Yang 1984).

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