The Heavy Metal Plants Metallophytes

A botanist can immediately identify a habitat as heavy metal soil polluted by high concentrations of Zn, Pb or other heavy metals by the composition of the plants. In Central Europe, most heavy metal soils carry four to six typical metallophytes. Highest Zn-concentrations are endured by spring sandwort (Minuartia (Alsine) verna, Fig. 2.1h) of the Caryophyllaceae which otherwise occurs only, although abundantly, on chalk meadows and rocks in alpine regions of Europe above the timberline. The thrifts or sea pinks (Armeria maritima) of the Plumbaginaceae form a somewhat difficult plant complex. The subspecies A. maritima ssp. halleri (Fig. 2.1f) grows only on heavy metal heaps in European plains, and can be differentiated morphologically only with difficulty from the subspecies maritima of the coastal salt marshes or the alpine ssp. alpina. The genus Armeria does not appear to be finally resolved taxonomically which is also true for its occurrence in different plant associations (Becker and Dierschke 2008). The same applies to pennycresses of the Brassicaceae (Thlaspi alpestre agg.) on heavy metal soils (Koch et al. 1998). Thlaspi caerulescens (Fig. 2.1k) and T. praecox form ecotypes on heavy metal heaps. The plants on some heavy metal locations are often termed

Metallophytes
Fig. 2.1 (Continued)

T. caerulescens ssp. calaminare, but the differentiation to T. montanum and the "genuine" T. alpestre is not always obvious. A revision has recently been made on the genus Thlaspi; T. caerulescens is now supposed to be Noccaea caerulescens

Fig. 2.1 A selection of European heavy metal plants. (a) A meadow on a Zn-rich heavy metal heap at Schlangenberg/Stolberg close to Aachen, Germany. The yellow zinc violet (Viola lutea ssp. calaminaria) dominates and also Armeria maritima ssp. halleri is detectable as red flowering spots. Photo from June 1998. (b) The blue-zinc violet (Viola lutea ssp. westfalica) occurs only in the Pb-ditch and its surrounding heaps at Blankenrode close to Paderborn, Germany. The photo also shows Cardaminopsis (Arabidopsis) halleri (white flowers) at this location. May 1987. (c) The blue-zinc violet (Viola lutea ssp. westfalica also grows happily on nonpolluted soils. Photo from the author's own allotment at D-Erftstadt. June 2009. (d) The alpine Viola lutea is the ancestor of the zinc violets (Hildebrandt et al. 2006). Zweisimmen/Bern, Switzerland. July 1997. (e) Viola tricolor forms specific ecotypes on heavy metal heaps. Siebertal, Harz mountains, Germany. June 1992. (f) Armeria maritima ssp. halleri from Schlangenberg/Stolberg close to Aachen. June 2002. (g) Silene vulgaris var. humilis which shows the bent shoots typical of the heavy metal ecotype of this plant species. Schlangenberg/Stolberg close to Aachen. June 2002. (h) Minuartia (Alsine) verna on heavy metal polluted gravel in the Gailitz river bed close to Arnoldstein, Southern Austria. (i) Thlaspi cepaeifolium on a heap close to a Zn-smelter at Cave del Predil (Raibl) in Northern Italy, close to the Slovenian border. This is an almost extinct species, but it is not related to Thlaspi caerulescens. May 2001. (j) Alyssum wulfenianum, an extremely rare heavy metal plant in the Gailitz river close to Arnoldstein, Southern Austria. May 2001. (k) Thlaspi caerulescens ssp. calaminare (=Thlaspi calaminare). Schlangenberg/Stolberg close to Aachen. April 2002. (1) Thlaspi goesingense from a serpentine soil at Pernegg/Mur in Steiermark, Austria. June 2002

(Meyer 2006). However, the taxonomy of the genus Thlaspi remains controversial (Koch et al. 1998) and it presumably is polyphyletic (Broadley et al. 2007). A separate tribe is the Ni-hyperaccumulator Thlaspi goesingense (Fig. 2.1l) which thrives on serpentine soils in South-Eastern European countries. This latter is fairly productive and could be a good candidate for phytoremediation purposes on heavy metal heaps.

The bladder campion (Silene vulgaris, Fig. 2.1g) of the Caryophyllaceae forms a characteristic ecotype on heavy metal heaps. Whereas the shoots of this plant are straight on nonpolluted soils, they are bent or curved in specimens found on heavy metal heaps (forma humilis). I express from my own experience of diverse heavy metal heaps in Germany, Poland and alpine areas in Austria, Slovenia and Italy that this is an indicative feature of the heavy metal ecotype. Any taxonomic relationship of the humilis ecotype to the alpine S. vulgaris ssp. prostrata does not appear to be resolved at present. S. vulgaris has frequently been used for physiological and biochemical studies on heavy metal tolerance (e.g. Schat and Tenbookum 1992; Schat and Vooijs 1997; Kovacik et al. 2010).

Haller's rockcress (Cardaminopsis halleri, Fig. 2.1b) is even more in the center of interest of experimental studies nowadays. It is closely related to the model plant of modern molecular biology, Arabidopsis thaliana, and therefore termed Arabidopsis halleri in recent publications (Koch and Matchinger 2007; Macnair et al. 1999; Meyer et al. 2009, 2010). The gene compositions of both Arabidopsis thaliana and Cardaminopsis halleri are similar, and molecular techniques to identify and manipulate the genes can be applied to both species (Pauwels et al. 2005; Willems et al. 2007; Roosens et al. 2008). In the field, Cardaminopsis halleri occurs on heavy metal heaps, but not when the content of heavy metals, particularly Cu, is high in soils (Becker and Dierschke 2008). In contrast to other metallophytes already mentioned, it escapes from heavy metal heaps to neighboring nonpolluted sites and is therefore sometimes called "pseudometallophyte" (e.g. Pauwels et al. 2005, 2006) and its abundance is positively affected by soil depth and moisture (Becker and Dierschke 2008).

My personal comment on the nomenclature Arabidopsis-Cardaminopsis may be added here. The former genus Cardaminopsis is now abandoned to Arabidopsis (Koch and Matchinger 2007). All members of the former Cardaminopsis possess eight chromosomes in the haploid state whereas A. thaliana has only five. Molecular information is based only on ITS and cpDNA sequencing but not on nuclear DNA properties. The evolutionary split between the x-5 A. thaliana and the x-8 Cardaminopsis occurred around 5 Ma (Bechsgaard et al. 2006), a long time ago. However, in all these considerations, morphological criteria are completely ignored. From knowing natural populations of A. thaliana and Cardaminopsis species (C. halleri, petraea, arenosa), I would immediately believe that Arabidopsis and Cardaminopsis belong to different genera, although, as is known, no absolute criteria exist to define a species or a genus. On the other hand, the juxtaposition of members of Cardaminopsis to the model plant A. thaliana places them more into the focus of current interest. The sequence identity between A. thaliana and C. halleri is around 94% (Becher et al. 2004). For comparison, chimpanzee and human share a sequence identity of 98.8% (Cyranowski 2001; Mikkelsen et al. 2005), so a common genus for both species might not be accepted by many people. Another relative of A. thaliana, the salt cress Thellungiella halophila, is 95% identical, at the cDNA level, but both genera are considered to be separate (Verbruggen et al. 2009).

Other plant ecotypes exist in Central Europe that are particularly adapted to a life on heavy metal soils. For example, a subspecies thriving on heavy metal heaps and termed Festuca aquisgranensis has been separated from the Festuca ovina aggregate (Patzke and Brown 1990). However, the Festuca ovina agg. is a fairly difficult taxon which is not yet finally resolved by morphological criteria. Other plants, particularly grasses (Bradshaw 1952; Wu et al. 1975; Humphreys and Nicholls 1984) may also have evolved heavy metal-adapted ecotypes (subspecies) which can, however, only be identified as separate species by current molecular techniques.

The zinc violets are special beauties (Fig. 2.1a) that occur only on heavy metal sites of very restricted distribution in Western Central Europe (Schwickerath 1944). The yellow zinc violet (V. lutea ssp. calaminaria) lives on Zn-rich soils in the area between Aachen, Germany and Liege, Belgium, and the blue form (V. lutea ssp. westfalica, Fig. 2.1b, c) thrives in a ditch and the surrounding heaps in an area of some 1 km x 0.5 km at Blankenrode, Eastern Westphalia, Germany. Both taxa belong to the most endangered plants in Central Europe and are probably the only unambiguous endemic taxa in Central Europe outside the alpine regions. Lack of competitiveness forces them to survive on heavy metal heaps. Molecular analyses showed that they are closely related to the alpine V. lutea (Fig. 2.1d) which occurs in Vosges or in the Sudeten mountains and more rarely in the Alps (Hildebrandt et al. 2006). The zinc violets might be relicts of the glacial period where they and their parents V. lutea seemingly had a wider distribution. Their patchy occurrence in Central Europe and also in Great Britain is an indication for such a history. Isolation on heavy metal heaps of the zinc violets may have resulted in the separation from their parents into the two separate entities.

In more Eastern and Southern European countries the zinc violets seem to be replaced by wild pansy (heartsease), Viola tricolor (Fig. 2.1e), which has developed ecotypes that can cope with fairly high concentrations of heavy metals (Slomka et al. 2011). This plant is, however, not restricted to heavy metal soils but occurs on gravel or sandy soils throughout the areas just mentioned.

When leaving Central Europe, the vegetation on heavy metal sites changes. Heavy metal soils in the area between Carinthia, Austria, Friaul in Italy and Northern Slovenia carry two very remarkable and almost extinct metallophytes: Alyssum wulfenianum (Fig. 2.1j) and Thlaspi cepaeifolium ssp. cepaeifolium (Fig. 2.1i) which is unrelated to the Thlaspi alpestre agg, mentioned above but has close taxonomic affinities to Thlaspi rotundifolium. The need to preserve these extremely rare metallophytes is obvious. A detailed account of the metallophytes and their role in plant associations particularly in Northern and Southern Europe is given by Ernst (1974), and a list of heavy metal plants of the world can be found in Brooks (1998) or Prasad and Hagemeyer (1999). It is estimated that approximately 500 angiosperms representing about 0.2% of all higher plants are metallophytes (Baker and Brooks 1989; cited in Kramer 2010).

A differentiation is often made between absolute (strict or eu-) metallophytes and facultative (pseudo-) metallophytes according to their occurrence either only on polluted sites or on both contaminated and noncontaminated habitats (Lambinon and Augier 1964; Willems et al. 2007). However, as just said, all metallophytes of Central Europe occur outside heavy metal sites. On their natural stands in the European plains, they cannot compete with faster growing plants on nonpolluted soils. Their patchy distribution in Europe may be the result of glacial epoques and the postglacial warm period. Such a differentiation between strict and pseudo-metallophytes is possibly justified at the subspecies level, for example for Viola lutea ssp. calaminaria and V. l. ssp. westfalica or Armeria maritima ssp. halleri on one side and V. lutea ssp. lutea or Armeria maritima ssp. maritima on the other. Such a differentiation merges into the discussion what is a subspecies in botany.

2.3 Accumulating and Hyperaccumulating Metallophytes

Heavy metal plants differ largely in their heavy metal contents as indicated by analysis of the plants that grew on a Zn-rich heavy metal soil close to Aachen, Germany (Table 2.1). Leaves of Thlaspi caerulescens (T. alpestre ssp. calaminare) and Minuartia verna contained the highest amount of Zn. The ratio between Cd and Zn is low in Minuartia verna and Silene cucubalus var. humilis in contrast to the situation in T. caerulescens. Armeria maritima in particular accumulates Pb. Thus

Table 2.1 Heavy metal content in mmol x kg-1 in leaves of plants living on the Zn-polluted soil at Breinigerberg close to Aachen, Germany

Plant species

Zn

Pb

Cd

Thlaspi alpestre ssp. calaminare

(=T. caerulescens)

159.0

8.21

4.83

Minuartia verna

151.3

6.52

0.65

Armeria maritima ssp. calaminaria

112.8

11.60

1.10

Silene cucubalus var. humilis

40.8

0.29

0.02

Plantago lanceolata

39.2

2.35

0.19

Lotus corniculatus

30.4

0.05

0.02

Anthyllis vulneraria

28.8

0.15

0.03

Festuca ovina

28.3

0.97

0.13

Campanula rotundifolia

24.8

4.70

0.98

Thymus serpyllum agg.

22.9

3.96

0.33

Cladonia rangifera (podetium) (lichen)

21.4

8.08

0.40

Rumex acetosa

21.4

2.12

0.16

Agrostis tenuis

17.4

0.88

0.10

Achillea millefolium

14.8

1.38

0.02

Euphrasia stricta

14.3

0.94

0.10

Viola lutea ssp. calaminaria

8.9

0.19

0.02

Pimpinella saxifraga

8.2

0.26

0.03

The data are taken from Ernst (1982). Extreme values are given in bold

The data are taken from Ernst (1982). Extreme values are given in bold there is no tolerance to heavy metal in general, but each metallophyte has evolved a strategy to cope with an individual heavy metal.

The amount of heavy metals taken up by a plant is dependent on the concentration of heavy metals in the polluted soil. In most plants, heavy metals are predominantly accumulated in roots. The shoot/root ratio is generally below unity in most plants but not in metallophytes. In some heavy metal plants, the concentration of heavy metals in shoots and leaves can be particularly high and the partitioning of heavy metals between shoots and roots differs from one metallophyte to the next and with each individual heavy metal (Kramer 2010).

The zinc violet V. lutea ssp. calaminaria has very low amounts of Zn, Pb, and Cd in its leaves (Table 2.1). Although conflicting data have been published on the levels of heavy metals in zinc violets (Jedrzejczyk et al. 2002; Noret et al. 2007), these violets have distinctly less heavy metals in their organs and thus show a different pattern of adaptation to heavy metal stress in soils than Thlaspi caerulescens, Minuartia verna, or Armeria maritima. The two basic strategies to respond to heavy metal toxicity emerge from the comparison of the data of Table 2.1. Metallophytes can be either excluders of heavy metals or they can be accumulators (Ramirez-Rodriguez et al. 2005). The zinc violet is a good example of an excluder. The other three species mentioned (Thlaspi, Minuartia, and Armeria) are accumulators. Some plants are hyperaccumulators, however, only for a single or few specific heavy metals. Thlaspi caerulescens, Cardaminopsis halleri, and the Crassulaceae Sedum alfredii (Sun et al. 2007) hyperaccumulate Zn and Cd, but not Pb (Broadley et al. 2007). The Katanga species Haumaniastrum katangense is a hyperaccumulator for copper (Chipeng et al. 2010). The Ni-hyperaccumulating species Alyssum murale (Ernst 2005), Alyssum bertolonii (Boominathan et al. 2004), Berkheya coddii (Robinson et al. 2003), or several endemic species of the serpentine flora of Zimbabwe (Brooks and Yang 1984) were suggested as potential enrichers of this element for human exploitation (leaching purposes). The fern Pteris vittata accumulates Se from seleniferous soils (Liao et al. 2004) and the violet Viola baoshanensis is a Cd-hyperaccumulator (Wu et al. 2010). Hyperaccumulators of Pb do not seem to exist (or are rare) due to the fact that Pb is extremely immobile and is not easily accumulated by plants (Bert et al. 2002). An extreme example for hyperaccumulation is Sebertia acuminata which can store up to 26% (w/w) Ni in its latex (Jaffre et al. 1976; Verbruggen et al. 2009).

The degree of tolerance of plants to heavy metals was divided into the three categories: hypotolerance, basal tolerance, and hypertolerance in a more recent review (Ernst et al. 2008). Although some plant species are clear hyperaccumulators for Cu, Zn or Cd, no species can store excess of all heavy metals. The borderline between basal tolerance and hyperaccumulation is blurred. A hyperaccumulator may be defined by the threshold value which is approximately a 10 times higher concentration of a heavy metal in the aerial parts compared to the content in a nonhyperaccumulator growing on the same polluted habitat (Bert et al. 2002). Approximately 400 taxa worldwide are hyperaccumulators (Bert et al. 2002). To give more precise values a Zn hyperaccumulator is defined as a plant that contains >10,000 mg g 1 dry weight (1%, w/w), and a Cd hyperaccumulator should have >100 mg g^1 dry weight (0.01%, w/w) (Baker 1981; Bert et al. 2002).

Halophytes can be divided into salt-resistant and salt-tolerant species. Salicornia europaea and Suaeda maritima need a high soil concentration of NaCl for germination and growth and are therefore salt-resistant species. All other halophytes grow better in non-NaCl enriched soils (gardens) than in saline habitats and are therefore salt-tolerant (Hildebrandt et al. 2007). All metallophytes of Central Europe are metal-tolerant (Hildebrandt et al. 2007). Lack of competitiveness forces them to live on heavy metal soils where they are not overgrown by more productive glycophytes. This is also true of the blue-zinc violet (V. lutea ssp. westfalica) where its germination and growth was claimed to require polluted soils with excess of heavy metals (Nauenburg 1986). The blue-zinc violet was shown to grow with no impaired vitality in garden soils at several locations in Germany in the last years. Its germination requires darkness, but is even more effective in nonpolluted garden earth than in heavy metals soils (Slomka et al. 2011). I am not aware of any clear-cut heavy-metal-resistant plant species worldwide that would be strictly dependent on the presence of excess of heavy metals in its growth substratum.

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