CHAPTER TWO
Metallophytes: the unique biological
resource, its ecology and conservational
status in Europe, central Africa and
Latin America
ALAN J. M. BAKER, WILFRIED H. O. ERNST,
ANTONY VAN DER ENT, FRANC¸OIS MALAISSE
AND ROSANNA GINOCCHIO
Introduction
Metalliferous soils provide very restrictive habitats for plants due to phytotoxicity,
resulting in severe selection pressures. Species comprising heavy-metal plant
communities are genetically altered ecotypes with specific tolerances to,
e.g., cadmium, copper, lead, nickel, zinc and arsenic, adapted through micro-
evolutionary processes. Evolution of metal tolerance takes place at each specific
site (Ernst 2006). A high degree of metal tolerance depends on the bioavailable
fraction of the metal(loids) in the soil and the type of mineralization. At extremely
high soil metal concentrations, especially on polymetallic soils, even metal-tolerant
genotypes are not able to evolve extreme tolerances to several heavy metals
simultaneously. Adapted genotypes are the result of the Darwinian natural selec-
tion of metal-tolerant individuals selected from surrounding non-metalliferous
populations (Antonovics et al. 1971; Baker 1987; Ernst 2006). Such selection can
lead ultimately to speciation and the evolution of endemic taxa. Heavy-metal
tolerance was first reported by Prat (1934) in Silene dioica and demonstrated experi-
mentally in grasses by Bradshaw and co-workers in Agrostis spp. and by Wilkins
in Festuca ovina in the late 1950s and 1960s (see Antonovics et al. 1971) and from
the early 1950s onwards in the herb Silene vulgaris by Baumeister and co-workers
(see Ernst 1974). Metal-tolerant plants avoid intoxication by an excess of heavy
metals by means of special cellular mechanisms, as long as the soil metal levels
do not exceed the levels of metal tolerance (Ernst 1974; Ernst et al. 2004). They
can thus thrive on soils that are too toxic for non-adapted species and ecotypes.
These unique plants with an ability to tolerate metal toxicities and survive and
reproduce on metalliferous soils are called metallophytes.
Ecology of Industrial Pollution, eds. Lesley C. Batty and Kevin B. Hallberg. Published by Cambridge
University Press. # British Ecological Society 2010.
(a)
(b)
Figure 2.1. Metallophyte vegetation on ancient lead-mining sites in the UK. (a) Sparse
cover of Agrostis capilliaris and Silene uniflora on acidic wastes at Goginan lead mine,
central Wales; (b) Continuous metallophyte turf colonising superficial mine workings
at Gang mines, near Matlock, Peak District. The calcareous substrate here and mosaic of
metal contamination levels produce a rich assemblage of metallophytes including
Minuartia verna in the most metal-contaminated areas. Photos: A. J. M. Baker. See colour
plate section.
8 ALAN J. M. BAKER ET AL
Heavy-metal sites and their vegetation in Europe
Evolution and distribution of metallophytes
After the last Quaternary Ice Age, forest developed on nearly all soils in Europe,
except on those with extreme climatic or edaphic conditions. In the latter group
are soils with elevated concentrations of heavy metals, too toxic for trees. In such
situations, shadow-sensitive xerophytes were able to survive when they had the
genetic advantages in metal tolerance (Ernst et al. 1992). Heavy-metal-tolerant
vegetation was originally restricted to natural outcrops of metal ores, scattered
as a relic of the Late Glacial epoch over Europe. Most of these habitats were
destroyed or modified by mining activities from the Bronze Age onwards. How-
ever, metal mining has considerably enlarged the potential habitat range by
creating further areas of metal-contaminated soils (Ernst 1990; Ernst et al. 2004).
In Europe, sparsely distributed sites with metal-enriched soils form residual
sanctuaries for metallophyte communities. Most sites are disconnected spatially
and are of very limited extent. The UK has many sites in Wales (Davies & Roberts
1978), the Peak District (Barnatt & Penny 2004) and the North Pennines, and
some isolated sites in Cornwall and in the Mendips (Ernst 1974; JNCC 2002). The
central part of Germany is well-known for its heavy-metal vegetation (Schubert
1953, 1954; Ernst 1964, 1974; Becker et al. 2007). Alluvial heavy-metal vegetation
occurs along the rivers Innerste and Oker in the Harz Mountains. In the Mansfeld
area, several hundreds of large Cu-Pb-Zn-mine spoil heaps are scattered with metal-
lophyte communities (Schubert1953; Ernst &Nelissen 2000). Inthe European Alps in
Austria, Slovenia and Italy, in the French Pyrenees, and several small sites are known
in the Spanish Picos de Europa. The most studied and extensive communities are
those of the three-border area of Belgium, the Netherlands and Germany, the Harz
Mountains area and the Pennine orefield in the UK. Metallophyte vegetation makes
up an important component of the biodiversity of Europe (Whiting et al. 2004).
Thalius (1588) was the first to recognise a relationship between the plant
Minuartia verna and heavy-metal-enriched soils in the Harz Mountains, Germany.
Subsequently, the association of the plant with lead-mine wastes in the Pennine
orefield, UK, gave rise to its local name ‘leadwort’. Schulz (1912) speculated that
M. verna is in fact a glacial relict species surviving on heavy-metal soils as an
isolated population; this was later confirmed by genetic analysis (Baumbach
2005). Libbert (1930) then defined the Armerietum halleri as a plant association
specific to metalliferous soils, and the Violetum calaminariae was described from
the Breiniger Berg near Aachen by Schwickerath in 1931. Plant associations
specific to metal-enriched soils were thus recognised.
Types of heavy-metal sites
The history of metal sites determines the species composition of the vegetation.
Three types of heavy-metal vegetation can be distinguished on syntaxonomy
and on their occurrence: primary, secondary and tertiary.
METALLOPHYTES: THE UNIQUE BIOLOGICAL RESOURCE 9
Primary sites
Primary sites are those with metallophytes where elevated concentrations
of metals are due to natural mineralisation or ore outcropping, and not that
which is anthropogenically influenced. Primary sites in Europe are therefore
extremely rare today and mostly found as very patchy small sites in Central
Europe, in the Pyrenees and in the Alps (Ernst 1974). Virgin sites like those in
tropical woodlands and rainforests (Duvigneaud 1958; Brooks et al. 1985) are
virtually non-existent, although many of the African sites are also threatened
by mining activities (Leteinturier et al. 1999). Besides a high concentration of
metals like zinc, lead, cadmium or copper in soil, heavy-metal vegetation types
are characterised by a low nutrient availability. Hence, these plant commu-
nities are of very low productivity.
Secondary sites
Almost all primary metal-enriched sites in Europe have been anthropologically
influenced by mining activities. These secondary sites result from mining
activities, e.g., disturbed primary sites, spoil and slag heaps, ore processing
and concentration (beneficiation) areas. The distinction between primary and
secondary is often difficult to elaborate especially with ancient sites. Early
mining has diminished most primary occurrences of metallophytes. From the
Bronze Age to the late Middle Ages mining had a relatively low impact on the
local environment. Metallophytes occurred locally on primary sites, and super-
ficial mining created secondary habitats. Both habitat types were ecologically
very similar. At that time mining was restricted to areas with metals outcrop-
ping. After the Middle Ages, much larger secondary habitats were created,
often far away from areas with primary habitats, by deep underground mining
or by metal refining on site. Exceptionally high concentrations of metals in
soils at primary habitats result from weathering of natural mineralisation on
well-developed soils. Modern secondary habitats, however, have a totally differ-
ent substratum; mining has created soils with altered metal composition,
depleted phosphorus and organic matter concentrations and low water reten-
tion capacity. Besides evolving metal tolerance, plants growing on these wastes
were co-selected for tolerance to P-deficiency, resistance to drought and an
ability to grow on loose substrates (Ernst 2000). This has affected the edaphic
conditions and is a major cause of differences between primary and early
secondary habitats.
Tertiary sites
Tertiary metal vegetation types can be subdivided into those communities
whose genesis is a result of atmospheric deposition in the vicinity of metal
smelters or alluvial deposition of metal-enriched substrates by sedimentation
10
ALAN J. M. BAKER ET AL
in river floodplains and on raised riverbanks. Tertiary atmospheric habitats
originate by an input of a surplus of metals in a non-metal-enriched environ-
ment by industrial emissions (Baumbach et al. 2007) often far way from primary
sites supporting metallophyte populations. They are often strongly influenced
by acidification (by co-emission of sulphur oxides) whose effects are stronger
than those of metals in soil. Species occurring at such sites have been selected
from the local non-metal-enriched environment. These sites are frequently
species-poor, e.g., monocultures of those grass species which have the ability
to rapidly evolve metal tolerances such as: Agrostis stolonifera at the copper
refinery at Prescot, England (Wu et al. 1975); A. capillaris at the Cd/Zn smelter
at Budel, the Netherlands (Dueck et al. 1984); and Agropyron repens at the copper
smelter at Legnica, Poland (Brej 1998). Sometimes metallophytes have arrived
at smelter sites with the ores: an example is the moss Scopelophila cataractae
in Wales and in the Netherlands (Corley & Perry 1985; Sotiaux et al. 1987).
An unintentional introduction of Armeria maritima subsp. halleri into the Littfeld
area (Germany) may have been caused by mine workers when moving from
the Harz area to new mining sites (Ernst 1974). Such ‘transport endemism’
(Antonovics et al. 1971) has probably been a major reason for the extended local
distribution of metallophytes, such as Thlaspi caerulescens and Minuartia verna
in the Pennine orefield, UK. Frequent visits by botanists may be the reason
for the import of T. caerulescens to the Overpelt Zn/Cd smelter site in Belgium
and to its extended distribution in the Peak District, UK. Revegetation of
tailings with poplar trees in the Auby smelter area in France was not successful;
therefore, in the 1920s and in the 1950s Arabidopsis halleri and Armeria maritima
subsp. halleri were introduced from Central European calaminarian grassland
(Dahmani-Mu
¨
ller et al. 2000), and still show a good performance on the metal-
contaminated soils around the Auby smelter (Bert et al. 2000).
Tertiary alluvial habitats are more of a natural kind and are generally
species-rich, because they originate as a result of metal loadings to well-
developed soils in riverine systems, often close to primary and early secondary
sites (Van der Ent 2007). Downstream of mining activities, riverbanks have
been flooded with metal-enriched materials and seeds of metallophytes
since the Middle Ages in the Tyne valley, England (Macklin & Smith 1990),
in the Innerste and Oker valley in Germany (Libbert 1930; Ernst 1974; Ernst
et al. 2004) and in the Geul valley in the Netherlands (Kurris & Pagnier 1925).
Due to leaching of heavy metals from the surface soils, the survival
of this alluvial heavy-metal vegetation type depends on irregular metal rep-
lenishment by incidental riverbank flooding, such as in the Tyne valley
in 1986 (Rodwell et al. 2007), and in the Innerste and Oker Valley in 1969
(Ernst 1974) and 2007 (Klein & Niemann 2007). These heavy-metal-enriched
sediments not only affect agricultural crops in other parts of the riverbank
lands (Von Hodenberg & Finck 1975), but also transfer propagules from
METALLOPHYTES: THE UNIQUE BIOLOGICAL RESOURCE 11
