Abstract
The paper summarizes literature on climate, soil chemistry, vegetation and metal accumulation by plants found on ultramafic substrata in the circumboreal zone (sensu Takhtajan, Floristic regions of the world, 1986) of the Northern Hemisphere. We present a list of 50 endemic species and 18 ecotypes obligate to ultramafic soils from the circumboreal region of Holarctic, as well as 30 and 2 species of Ni and Zn hyperaccumulators, respectively. The number of both endemics and hyperaccumulators are markedly lower compared to that of the Mediterranean and tropical regions. The diversity of plant communities on ultramafics soils of the circumboral region is also described. The underlying causes for the differences of ultramafic flora between arctic, cold, cool temperate and Mediterranean and tropical regions are also discussed.
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Introduction
The uniqueness of vegetation growing on ultramafic (serpentine) soils has long been discussed (Brooks 1987; Baker et al. 1992; Roberts and Proctor 1992; Rajakaruna et al. 2009; Galey et al. 2017). The most thoroughly studied ultramafic vegetation are those of Mediterranean and tropical regions where the communities are characterized by low productivity and reduced floristic diversity compared to those on non-ultramafic soils (Pichi-Sermolli 1948; Harrison and Rajakaruna 2011). Ultramafic habitats of Mediterranean and tropical regions are home to unique plant communities (Galey et al. 2017), often rich in endemic species and subspecies as well as specific morphological and ecological forms (i.e. ecotypes; O’Dell and Rajakaruna 2011). Ultramafic soils are unique in harboring both basicolous and acidicolous species and the ultramafic flora often has a relatively xerophytic character and is dominated by certain families (Rune 1953).
Ultramafic rocks are widely distributed in the circumboreal region of the Northern Hemisphere and represented in the British Islands, Scandinavia, Central and Southern Europe, Ural Mountains, Altai, Chukotka, Hokkaido, Alaska, Northeast USA, northwestern US and adjacent Canada, and north- and southeastern Canada (Brooks 1987; Roberts and Proctor 1992). However, the literature on ultramafic vegetation and soil of this region is scant. This is a consequence of dispersed location, patchiness of exposed habitat, remoteness and poor accessibility of ultramafic massifs. The most thorough treatments available to date are of ultramafic vegetation in the Scandinavian region (Rune 1953; Rune and Westerberg 1992; Nyberg Berglund et al. 2004) and eastern North America (Rajakaruna et al. 2009). Some ultramafic communities in Britain (Proctor 1992), including the Lizard peninsula in England and outcrops in Anglesey, Wales (Proctor and Woodell 1971), Scotland (Steele 1955), Cornwall (Coombe and Frost 1956a, b) and Unst outcrop in Shetland (Spence 1957, 1958, 1959; Shewry and Peterson 1976; Carter et al. 1987) and Ireland (Brearley 2018) have also received some attention.
Studies in North America include those of the Alaska region, part of the Circum-Pacific orogenic belt, along the northern Pacific coast of USA (Alexander 2004; Alexander et al. 2007), the Appalachian Mountains of eastern North America (Rajakaruna et al. 2009; Burgess et al. 2015; Flinn et al. 2017), Southern British Columbia (Lewis and Bradfield 2004; Lewis et al. 2004), Gaspé Peninsula in Québec (Sirois and Grandtner 1992) and the Island of Newfoundland (Roberts and Proctor 1992) in Canada.
Ultramafic flora of Europe focus on ultramafic outcrops in the Balkan Peninsula (Tatić and Veljović 1992; Bani et al. 2010), and the North Caucasus (Drozdova et al. 2013; Alekseeva-Popova et al. 2015). Studies in the Eastern part of Eurasia include those in the ultramafic mountains occurring in the Polar region (Alekseeva-Popova 1970; Yurtzev et al. 2004; Proctor et al. 2005; Kholod 2007), Northern (Kulikov and Kirsanova 2012), Middle and Southern Urals (Teptina and Paukov 2012, 2015), Chukotka (Drozdova and Yurtzev 1995; Drozdova and Alekseeva-Popova 1999) and Japan (Mizuno and Nosaka 1992; Sakaguchi et al. 2017).
Scattered data and the wide range of climatic and orographic conditions do not give a complete picture of the peculiarities of ultramafic floras of arctic, cold and cool temperate climate; however, it is known that unlike those of regions with Mediterranean and tropical climate, they usually do not bear such distinct differences in comparison with their surrounding vegetation (Proctor 1999). They are additionally characterized by low endemism (Kruckeberg 2002) and relatively low number of hyperaccumulator species (Baker and Brooks 1989). In order to highlight the unique attributes of ultramafic vegetation in the circumboreal region, we present an overview of the literature on the ultramafic vegetation of the arctic, cold and cool temperate regions of the Northern Hemisphere.
Delimitation of the region
We have chosen three approaches for delimitation of the territory under consideration. The primary consideration is based on the floristic criteria used by Takhtajan (1986). This is used in order to demonstrate the floristic and genetic affinity of the flora of the territory. We follow the nomenclature of Takhtajian who used the term “circumboreal” for this region. Much of the Northern Hemisphere belongs to the Circumboreal floristic region of Holarctic which includes almost entire Russia except for the Far East south to the river Amur; northern Mongolia, Caucasus (except Talysh), Europe (except for the Mediterranean region), USA and Canada north to the oblique line, connecting New Scotland and Kenai Peninsula, Alaska and Aleutian Islands.
The second step was the delimitation of vegetational types within the circumboreal region and defining borders including similar types on both continents. The outlined region includes the Arctic deserts to broadleaf forests or mixed forests in continental regions (Adams 2007).
According to Köppen climate classification, the region under consideration covers areas with hemiboreal, boreal and polar climates (Peel et al. 2007). The climate of the territory is characterized by long and cold (below freezing point) winters, short and cool to warm summers, limited annual precipitation which exceeds evaporation and the absence of dry seasons. The warmest region under consideration is associated with cool temperate climate (Cfb and Cfc in the Köppen climate classification), whereas the coldest are subarctic (Dfc), extremely cold subarctic (Dfd) and polar (ET) climate. Intermediate conditions are characterized as humid continental climate (Dfb) (Table 1).
Elemental concentrations in ultramafic soils
Peculiarities of the climatic regime of the circumboreal region affect the processes of soil formation and chemical and physical characteristics of ultramafic soils. Ultramafic soils pose stressful conditions for plant growth. They are generally nutrient-poor (infertile), contain small amounts of most essential nutrients, such as nitrogen, potassium, phosphorus and calcium (Ca), and have high concentration of iron (Fe), magnesium (Mg), nickel (Ni), chromium (Cr) and cobalt (Co) (Proctor and Woodell 1975; Kruckeberg 1984; Brooks 1987; Roberts and Proctor 1992; Brady et al. 2005; Kazakou et al. 2008).
Skeletal soils on serpentinites are characterized by low plant nutrients, particularly phosphorus and potassium as reported for Great Britain (0.02%, Proctor and Woodell 1971). Potassium is also low in the soils of Newfoundland (0.03–0.39%, Roberts and Proctor 1992), Japan (0.02–4.7%, Mizuno et al. 2009), and Middle and Southern Urals (0.02–0.43%, Teptina and Paukov 2015). Low quantities of potassium are also reported in the Polar Urals (Proctor et al. 2005; Kataeva 2013), Chukotka (Drozdova and Yurtzev 1995; Drozdova and Alekseeva-Popova 1999), and North America (Alexander 2004). Unlike skeletal soils, ultramafic soils under a canopy of vegetation are distinct by having relatively higher concentrations of major nutrients (Proctor and Woodell 1971).
Ultramafic soils usually contain elevated concentrations of trace elements such as Ni, Co, and Cr, which are toxic to most plants. Ni concentrations in the circumboreal region commonly vary from 100–2600 µg g−1, much lower compared to tropical regions which average 500–5000 µg g−1 (Reeves et al. 1996; Reeves and Baker 2000). Higher concentrations of total Ni were recorded in a few sites in Hokkaido (2590 µg g−1 Ni), Polar Urals (2830 µg g−1 Ni) and for skeletal soils in Newfoundland (3980 µg g−1 Ni). Exceptionally high concentrations were reported by Proctor (1992) and Carter et al. (1987) for Unst and Shetland ultramafic sites, respectively, in Great Britain (up to 9700 µg g−1 Ni).
Territories situated to the south of the circumboreal region similarly do not contain extremely high concentrations of total Ni. Examples include Albania 54–3579 µg g−1 (Shallari et al. 1998; Bani et al. 2010), Northern Greece (1160–2660 µg g−1; Bani et al. 2010), Bulgaria (2333–3278 µg g−1; Bani et al. 2010), and Iran (310–1775 µg g−1; Ghaderian et al. 2007a, b) (Fig. 1). There is no particular trend for total Ni in ultramafic soils depending on latitude or climatic group, but may rather depend on the chemistry of underlying parental rocks.
Data on available and exchangeable Ni in soils of different localities are not exhaustive to make a comprehensive conclusion on its dependence on climatic factors; however, soils in localities which belong to the circumboreal region contain less available and more exchangeable Ni compared to more southern sites situated in Iran or in the Mediterranean region (Fig. 2).
Content of other metals in soils of circumboreal zone is likewise highly variable and may reflect the peculiarities of chemical composition of ultramafic rocks. Chromium content in soils vary dramatically: 50–19,100 µg g−1 in Britain (Proctor 1992), 55–523 µg g−1 in the Southern and Middle Urals (Teptina and Paukov 2015) and 91–3865 µg g−1 in Albania (Shallari et al. 1998; Bani et al. 2010), 1110–2170 µg g−1 in Greece (Bani et al. 2010), 1785–3870 µg g−1 in Bulgaria (Bani et al. 2010), and 36–365 µg g−1 in Iran (Ghaderian et al. 2007a, b)
A ten-fold difference was found between the lowest and the highest concentrations of total Fe and Co in ultramafic soils between arctic, cold, cool temperate and Mediterranean regions. The northernmost localities contain less total Fe, Ca and Co (Figs. 3, 4). However, similarity of Fe and Co in ultramafic soils of Iran and Middle Urals may reflect its dependence on the features of underlying rocks.
Generally reduced Ca is another distinguishing feature of ultramafic soils, as emphasized in studies of Proctor and Woodell (1971) and others (Rajakaruna et al. 2009; Galey et al. 2017). It is generally less than 1% (often with a Ca:Mg molar quotient of < 1), however, Ca concentrations may vary from very low (0.11% in Albania) to fairly high (7% in Britain). Conversely, Mg is prevalent in all ultramafic soils of circumboreal region, including 0.8–5.4% in the Southern and Middle Urals (Teptina and Paukov 2015), 0.16–0.17% in Maine (Pope et al. 2010), 11–26% in Japan (Mizuno et al. 2009), 13–19% in Bulgaria (Bani et al. 2010), and 10–16% in Iran (Ghaderian et al. 2007a, b).
Vegetation
The flora of the region under consideration is extremely heterogeneous, often resulting from extreme localisation, climate, orography and other abiotic and biotic factors. Even in regions with the same climate there is a significant heterogeneity with respect to ultramafic associated vegetation (Rune 1953; Proctor 2003).
In the global scale, vegetation communities of ultramafic soils vary from wet bogs and different types of forests to steppe and open, outcrop communities. Within the circumboreal region, the features of ultramafic vegetation are determined by geology, climate and relief. Rune (1953) noted that the vegetation of ultramafics, even within a small region such as Northern Sweden, is not uniform, varying from grasslands and forests to open, rock outcrop communities.
Despite numerous studies on the significant contrast of vegetation between ultramafic and non-ultramafic sites in regions with Mediterranean and tropical climates (reviewed in Kruckeberg 1992; Roberts and Proctor 1992; Galey et al. 2017), such differences in vegetation of ultramafics in arctic, cold and cool temperate regions are not well known. Plant communities on the ultramafic outcrops in Britain and Shetland essentially do not have any soil-specific features (Coombe and Frost 1956a, b; Spence and Millar 1963; Spence 1970). A weak contrast in the structure and species composition on ultramafic and granite outcrops of Deer Isles, Maine was, however, noted (Pope et al. 2010). On developed soils on flatlands, vegetation is often represented by zonal communities, devoid of unique features, as in the Urals Mountains (Teptina and Paukov 2012) and in the Czech Republic (Chytrý 2012).
On undeveloped soils, which are formed on slopes, summits of mountains and river banks, the influence of underlying rocks is greater. Rune (1953) notes the presence of sharp division between ultramafic and non-ultramafic vegetation of coastal districts in Norway and on Mt. Albert in Québec (Rune 1954). Chitrý (2012) reports a marked shift of Fagus sylvatica- and Carpinus betulus-dominated communities by Pinus sylvestris or Quercus petraea forests on shallow ultramafic soils.
Syntaxonomical revision of plant communities on ultramafic bedrocks allows describing unique, often endemic ultramafic associations (Roberts and Proctor 1992; Stevanović et al. 2003; Alexander et al. 2007). Numerous phytosociological studies have been conducted for ultramafic vegetation of Mediterranean region of California (Rivas-Martínez 1997; Rodríguez-Rojo et al. 2001a, b; Sánchez-Mata et al. 2004; Sánchez-Mata and Rodríguez-Rojo 2016).
Comparatively little data exist on the diversity of ultramafic communities in cool temperate sites of the Balkan region. Several associations, which belong to the endemic order Halacsyetalia sendtneri, were discribed from the eastern and central part of ultramafic grasslands of western Balkans (Ritter-Studnička 1970) and from the south-eastern part of Kosovo (Blečić et al. 1969; Jovanović et al. 1992; Millaku et al. 2011). The associations from Kosovo belong to alliance Centaureo–Bromion fibrosi. Thorough investigations of ultramafic grasslands in Bulgaria and similar communities of regional countries have resulted in one new endemic association, Onosmo pavlovae–Festucetum dalmaticae, which is included in Alyssion heldreichii alliance occuring on ultramafic outcrops in northern Greece (Janišová et al. 2011; Vassilev et al. 2011; Tzonev et al. 2013).
Ultramafic vegetation of rocks and screes in the Czech Republic was assigned to the class Asplenietea trichomanis, order Asplenion cuneifolii (Chytrý 2012) and the class Asplenietea trichomanis, alliance Cystopteridion (Vicherek 1970). Chasmophitic vegetation of ultramafic cliffs was included in the alliance Asplenion serpentini. Communities of dry ultramafic grasslands included in the alliance Asplenio cuneifolii–Armerion serpentini (Chytrý and Tichý 2003). Similarly, in Serbia, 19 associations were described on ultramafic soils and scree slopes (Jovanović et al. 1986; Lakušić and Sabovljević 2005), which were assigned to the alliance Centaureo–Bromion fibrosi and order Halacsyetalia sendtneri. One of these associations, Stipetum novakii, occurs on open rocky ultramafic grasslands in Brdjani Gorge (Kabaš et al. 2013).
On ultramafic outcrops of the Middle Urals, one association (Pulsatillo uralensis–Helictotrichetum desertorum) with two subassociations (P. u.–H. d. calamagrostietosum arundinaceae, P. u.–H. d. calamagrostietosum epigeii) were described (Teptina et al. 2018). The communities were assigned to the alliance Helictotricho desertorum–Orostachyion spinosae, of the order Helictotricho-Stipetalia, and class Festuco-Brometea.
Ultramafic pine forests were assigned to the class Erico-Pinetea and alliance Erico-Pinion (Chytrý and Tichý 2003). Pine forests on ultramafics at lower altitudes in central Bohemia and south-western Moravia Sesleria caerulea are assigned to the class Erico-Pinetea and alliance Erico carneae–Pinion (Chytrý 2012).
Geoedaphic factors determine the composition of flora of ultramafic substrates worldwide (Rajakaruna and Boyd 2008). The unique character of ultramafic flora has been repeatedly emphasized by researchers in both tropical and temperate regions (Robinson et al. 1997; Reeves et al. 1999; Van der Ent et al. 2015; Galey et al. 2017). Ultramafic flora of tropical regions, especially on islands, is characterized by a high level of endemism, often reaching 90% (Anacker 2011).
In comparison with floras on other rock types, ultramafic vegetation, even in higher latitudes, differs by fairly low species diversity and abundance. For example, the ultramafic flora of Norway and Finland (Rune 1953, 1954) includes a small number of species and individuals. Similarly, impoverished species diversity and abundance were documented in the Polar Urals (Igoshina 1966) where the flora of ultramafic massif Rai-Iz is species poor in comparison to the flora of schist massif Yar-Keu. Comparative studies of plant diversity on ultramafic soils of Rai-Iz and Voikaro-Syninsky ultramafic massifs and acidic soils of Big Paipudinskiy massif in tundra zone of the Polar Urals have also showed low diversity of species on ultramafic soils (Alekseeva-Popova 1970; Yurtsev et al. 2001). In the Southern Urals, lower plant species diversity on ultramafic rocks (Sugomakskiy ultramafic massif) was observed in comparison with the species diversity of Vishnevogorskiy sienite massif (Teptina and Paukov 2012).
The cover and abundance of plants are mainly determined by the nature of the soil. Shallow ultramafic soils usually have extremely sparse vegetation. Proctor and Woodell (1971) note poor composition of the debris flora in Scotland, but note relatively high abundance of heath communities on ultramafics, which occur on more developed soils. Likewise, diversity of plants on well developed ultramafic soils in the Middle Urals is similar to that on other substrates (Teptina and Paukov 2012).
The flora of ultramafics in northern Eurasia is distinguished by the presence of Caryophyllaceae (Rune 1953; Teptina and Paukov 2012), a family that is characteristic of Holarctic floras (Malyshev 1972) and typical for petrophytic communities on initial successional stages on rock substrates (Rune 1953; Kinzel 1982). One characteristic feature of boreal serpentinite floras is the absence of distinct families and genera (Yurtsev et al. 2001; Teptina and Paukov 2012). For example, the ultramafic flora of the Southern Urals is often devoid of members of Fabaceae, mainly the genera Astragalus and Oxytropis.
Ultramafic ecotypes and endemic taxa
Ultramafic soils provide a favourable environment for the origin of new taxa and can be considered as “islands” sharply demarcated by distinct edaphic conditions. Adaptations of plant populations to such unique conditions and their further divergence in isolation lead to the formation of ecologically, physiologically and morphologically distinct populations which can be considered as different taxa, i.e., forms, varieties, ecotypes, subspecies and species endemic to ultramafic soils (Rajakaruna 2018).
Morphological differences between populations of plants on ultramafic and non-ultramafic soils appear in the form of serpentinomorphoses. They are often described as stenophyllism, glabrescence, glaucescence and nanism (Rune 1953; Kruckeberg 2002). The existence of ultramafic races has been repeatedly noted by many researchers (Novák 1928; Rune 1953; Kruckeberg 2002; O’Dell and Rajakaruna 2011). For instance, physiological and morphological races of plants have been documented on British ultramafics (Proctor and Woodell 1971; Proctor 1992), including Asplenium adiantum-nigrum L. (Aspleniaceae), Juniperus communis L. (Cupressaceae), and Minuartia verna (L.) Hiern. (Caryophyllaceae). Additionally, Proctor (1992) reported several races of species, which differ ecologically or even morphologically, including Plantago maritima L. (Plantaginaceae), Rubus saxatilis L. (Rosaceae), Rumex acetosa L. (Polygonaceae) (on the Keen of Hamar, Shetland), Minuartia verna (L.) Hiern. subsp. verna, and Juniperus communis L. subsp. communis (on the ‘Rock Heath’). Some ultramafic-associated varieties have also been described from ultramafics in Norway (e.g., Rumex acetosa L. var. serpentinicola, Lychnis alpina L. var. serpentinicola and Cerastium alpinum L. var. serpentinicola (Caryophyllaceae)) (Rune 1953), Canada, Québec (e.g., Cerastium arvense var. ophiticola) (Raymond 1955), Finland and Moravia (e.g., Cerastium vulgatum L. var. serpentini (Novák) Gartner) (Kotilanen and Salmi 1950), Scandinavia [e.g, Melandrium rubrum Garcke var. serpentini (Caryophyllaceae)] (Kruckeberg 2002). Investigation of ultramafic and non-ultramafic populations of Cerastium alpinum L. in Sweden and Finland (Nyberg Berglund and Westerbergh 2001; Nyberg Berglund et al. 2001, 2004) revealed differences in serpentine tolerance within the species and independent and multiple evolution of serpentine-tolerant populations (Table 2).
The main taxonomic problem associated with the numerous geoedaphic variants, subspecies and species, which were distinguished in the past, was that they were based only on information about occurrence on specific (ultramafic) bedrocks or their distinct morphological features. Many of these taxa need to be genetically examined to confirm if they are “good taxa.”
Numerous ultramafic floras of the world are characterized by a high level of endemism (Brooks 1987). This is particularly true for tropical and subtropical regions, where ultramafic soils are inhabited by a large number of endemic plant taxa, many of which have limited distribution and are often endangered (Skinner and Pavlik 1994; Galey et al. 2017). Approximately 3000 endemic taxa restricted to ultramafic soils are known, however, many of them occur in tropical and subtropical regions (Brooks 1987; Anacker 2011; Galey et al. 2017). The level of endemism of ultramafic floras of the southern Mediterranean regions such as California is also extremely high (Kruckeberg 2002; Safford et al. 2005; Alexander et al. 2007), and is also strongly manifested on island floras (New Caledonia, Cuba, Borneo: Borhidi 1992; Jaffré 1992; Galey et al. 2017).
Low levels of endemism have often been reported in ultramafic floras of the arctic, cold and cool temperate zone. The only endemic species in the United Kingdom—Cerastium nigrescens (H. C. Watson) Edmondston ex H. C. Watson is known from few ultramafic habitats in Scotland (Dennes 1845; Watson 1860; Brooks 1998). Further treatments permit use of the name C. nigrescens not only for Shetland populations but also for other Scottish and Scandinavian ones (Brummitt et al. 1987).
Endemics have not been recorded on serpentinites in the Polar Urals (Proctor et al. 2005). Yurtsev et al. (2001) also noted that new taxa in the rank of species and subspecies do not occur in the ultramafic flora of the Polar Urals. Further, in the Southern and Middle Urals, new species and subspecies endemic to ultramafic substrate have yet to be described (Teptina and Paukov 2012).
In other circumboreal regions the number of endemic taxa obligate to ultramafic soils is not high. Rajakaruna et al. (2009), Harris and Rajakaruna (2009), and Boufford et al. (2014) report several ultramafic endemics for eastern North America, including Adiantum viridimontanum C. A. Paris (Pteridaceae) (Fig. 5), Minuartia marcescens (Fernald) House (Caryophyllaceae), Symphyotrichum rhiannon Weakley and Govus (Asteraceae), and Packera serpenticola (L.) A. Löve and D. Löve (Asteraceae). There are some perennial endemics on the ultramafics within Cerastium in Balkan region (e.g., Cerastium alsinifolium Tausch, C. neoscardicum Niketić, C. smolikanum Hartvig), North America (C. velutinum Rafinesque var. villosissimum (Pennell) J. K. Morton) and on the British Isles (C. fontanum Baumg. subsp. scoticum Jalas and Sell).
The origin of neoendemics in the northern floras is often associated with polyploidy (Stebbins 1984). Polyploid forms have competitive advantages in extreme environments and is often typical for genera such as Alyssum and Cerastium. Comprehensive morphological, cytological, genetic and ecological analyses support the existence of two new endemic species restricted to ultramafic outcrops in the Czech Republic (Kaplan 1998; Kolář et al. 2015). Similarly, diploid and tetraploid species of Knautia serpentinicola Smejkal ex Kolář, Z. Kaplan, J. Suda et Štech (Caprifoliaceae) have been described in ultramafic areas in the Czech Republic and Germany. The diploid K. pseudolongifolia (Szabó) Żmuda is known from only one site in Krkonoše Mountains (Kolář et al. 2015). Another two neoendemic species, Cerastium alsinifolium Tausch and Minuartia smejkalii Dvořáková (Chitrý 2012), are known from Western Bohemia. Adiantum viridimontanum, endemic to ultramafic soils in Maine, Vermont, and Québec, is also considered to be an allotetraploid hybrid between A. aleuticum (Ruprecht) Paris and A. pedatum L. (Harris and Rajakaruna 2009).
Hyperaccumulation of trace elements
Ultramafic outcrops are home to over 500 species of Ni-hyperaccumulating plants, the majority of which are found in Mediterranean and tropical climates (Berazaín et al. 2007; Gall and Rajakaruna 2013; Sánchez-Mata et al. 2013). Many of these hyperaccumulating plants belong to seven territories—New Caledonia, Western Australia, southern Europe and Asia Minor, The Malay Archipelago, Cuba, western United States and Zimbabwe (Reeves 1970; Baker and Brooks 1989; Galey et al. 2017). In regions with arctic, cold and cool climates, the number of such species is not high. Ultramafic flora of cold regions is characterized by atypically low level of hyperaccumulator species (Table 3). Some ultramafic floras do not include such species at all; for instance, Proctor (1992) noted the absence of Ni-hyperaccumulating plants on ultramafic outcrops of Britain. The arctic and boreal regions affected by the glaciation events during the Pleistocene do not appear to harbor hyperaccumulator species (Brooks 1983, Baker and Brooks 1989); perhaps due to the lack of time for the evolution of such traits or reduced selection for hyperaccumulation.
Only genera Alyssum and Noccaea, which belong to Brassicaceae, are able to hyperaccumulate Ni in the circumboreal regions (Brooks and Radford 1978; Reeves and Brooks 1983). Nickel hyperaccumulation has been reported in Alyssum obovatum (C. A. Mey.) Turcz. in the Polar Urals (1000–4500 µg g−1) (Alekseeva-Popova et al. 1995; Proctor et al. 2005), Middle and Southern Urals (818–6003 µg g−1) (Teptina and Paukov 2015) and Chukotka (926–1308 µg g–1) (Drozdova and Yurtzev 1995; Drozdova and Alekseeva-Popova 1999). Alyssum obovatum is also known as a Ni hyperaccumulator in Alaska, USA and Canada (Brooks and Radford 1978; Brooks et al. 1979), although recent studies have not been undertaken to confirm these earlier findings.
Further to the south, the number of hyperaccumulator Alyssum species rise. Several other species from Alyssum have been reported as strong hyperaccumulators of Ni, such as Alyssum murale Waldst. and Kit. in the Northern Caucasus (Drozdova et al. 2013; Alekseeva-Popova et al. 2015), Bosnia and Herzegovina (Stamenković et al. 2017), Armenia (Doksopulo 1961) and Albania (Shallari et al. 1998) and Alyssum markgrafii O. E. Schulz ex Markgraf in Albania (Shallari et al. 1998).
The members of the genus Noccaea (Brassicaceae) are also characterized by their ability to accumulate Ni, as shown in Noccaea japonica (H. Boissieu) F. K. Mey. in Hokkaido, Japan (Mizuno et al. 2009), N. borealis F. K. Mey. in the Polar Urals (Alekseeva-Popova et al. 1995; Proctor et al. 2005; Al-Shehbaz 2014) and N. thlaspidioides (Pall.) F. K. Mey. in the Middle and Southern Urals (Teptina and Paukov 2015).
Some species from circumboreal region are also capable of hyperaccumulating Zn. For instance, Alyssum gehamense Halácsy in the Northern Caucasus (Drozdova et al. 2013), Noccaea caerulescens (J. Presl and C. Presl) F. K. Mey. in central Europe (Reeves and Brooks 1983) and Noccaea borealis in the Polar Urals have all been documented as accumulating Zn, but not reaching the hyperaccumulator threshold (Proctor et al. 2005).
Few species from families other than the Brassicaceae have been documented as hyperaccumulators of Ni, particularly members of Caryophyllaceae—Arenaria marcesens (Fernald) House in Western Newfoundland, Cerastium holosteoides Fr., C. nigrescens (H. C. Watson) Edmondston ex H. C. Watson, Sagina sp., Silene acaulis (L.) Jacq. and Plumbaginaceae—Armeria maritima (Mill.) Willd. in the Unst island (Shewry and Peterson 1976; Roberts and Proctor 1992). The records of Ni hyperaccumulation by members of other families, particularly Calluna vulgaris (L.) Hill. (Ericaceae) in the island of Unst (Shewry and Peterson 1976) and Solidago hispida Muhl. ex Willd. (Asteraceae) in western Newfoundland (Roberts and Proctor 1992) need to be verified.
Discussion
The question of why northern plant communities on ultramafic rocks often lack high levels of species endemism and are largely devoid of hyperaccumulators have long-intrigued serpentine ecologists. There are few explanations posed for why territories with arctic, cold and cool temperate climates are poor or devoid of obligate serpentinophytes and hyperaccumulators. The degree of endemism, in the opinion of Proctor (2003), depends on historical reasons, including climate, rather than purely on edaphic factors. These include recent glaciation and the ratio of precipitation and evaporation (Rune 1953; Proctor 1992). The last glaciation, which covered the territory of modern Canada, reached Black Sea and peaks of the Northern Urals (Baker and Brooks 1989; Kulikov et al. 2013), severely impacting colonization and subsequent evolution of plants. The endemic flora of these territories, which arose after the glaciers had retreated, can be considered as neoendemics (Kruckeberg 1986; Rajakaruna 2004; Anacker 2011). The flora of the Middle and Northern Urals has 88 (5.5% of total diversity) endemic species. Most of these plants are petrophytes and erosiophyles tolerant to open habitats and have evolved after the retreat of the last glacier (Kulikov et al. 2013), however, none of them is known as endemic to ultramafic soils. Tolerance to open (bare) habitats may be a prerequisite to formation of obligate serpentinophytes (Armbruster 2014; Cacho and Strauss 2014) and it is likely that in the northern latitudes this process is currently in its early stages, where subspecies, ecotypes, or races differing in edaphic tolerance or in their ability to hyperaccumulate Ni have yet to evolve as full-fledged species (Brummitt et al. 1987; Nyberg Berglund et al. 2004; Brysting 2008; Teptina and Paukov 2015). Territories in the Holarctic which have never been frozen bear high numbers of these species—at least 215 ultramafic endemic taxa are known in California, and the Mediterranean region is likewise rich in endemics (Anacker 2011). The only obligate serpentinophyte Alyssum litvinovii Knjaz. (Fig. 5b) is currently known from the Southern Urals but in the territory outside the circumboreal region (Knjasev 2011). Arid territories of Holarctic which have never been affected by glaciation processes may therefore represent a unique opportunity to discover new taxa which may qualify as obligate to ultramafic soils. These territories may include Mugodzhary mountains in Kazakhstan, Caucasus and Altai and are all worthy of intense field exploration.
Unlike in the tropics, where hyperaccumulation is known in many unrelated families, the hyperaccumulators in the northern territories belong mostly to Brassicaceae. The adaptive significance of metal hyperaccumulation has been discussed in detail (see Boyd 2014 for a discussion), pointing to elemental defense as a primary selecting agent in the evolution of metal hyperaccumulation. Some evidence suggests that some metals, including Ni, are physiologically essential for serpentinicolous plants (Ghasemi et al. 2014). Nickel may act as an osmoticum during drought stress (Baker and Walker 1990; Boyd 1998; Martens and Boyd 2002) or enhance reproductive fitness via increased flowering (Ghasemi et al. 2014). The high amounts of Ni may also act as defense from herbivores (Reeves et al. 1981; Ernst 1987; Boyd 2012). While the same factors hypothesized as driving the evolution of metal hyperaccumulation should apply wherever there are plants on ultramafic soils, the lack of time for the evolution of this trait (due to recent glaciation in the circumboreal regions) and reduced intensity of herbivore and pathogen damage (compared to warmer regions) may contribute to fewer hyperaccumulators in the northern climates.
One of the more adverse conditions on ultramafic soils is a constant lack of moisture, high insolation and a significant temperature drop on the soil surface (Proctor and Woodell 1975; Kruckeberg 1984; Brooks 1987; Brady et al. 2005). In the regions with arctic, cool and cold temperate climate, hyperaccumulators occur on shallow skeletal ultramafic soils, where there are significant periods of water deficiency or drought (Roberts and Proctor 1992; Hughes et al. 2001). Therefore, drought stress could likely drive the evolution of this trait and is worthy of examination via experimental studies. Interestingly, the number of hyperaccumulators rises southwards and, in continental regions, with the highest numbers found in the most arid regions. The species with wide latitudinal distribution in Holarctic such as Alyssum obovatum, which occurs in Eurasia, Canada and Alaska, may be useful in understanding this pattern.
The second reason may be the difference in the amounts of metals and their bioavailability in soils in circumboreal and tropical regions. Utramafic soils in Cuba and Brazil contain much higher Ni than any ultramafic soil of the Holarctic (Reeves et al. 1999, 2007). However, the cause and effect of reduced Ni in soil are difficult to demonstrate as there are only weak trends in the concentrations of metals in ultramafic soils in different climatic zones of the Holarctic (Figs. 1, 2, 3, 4). Further, it is difficult to find strong correlations between soil metal concentration and metal accumulation rates by plants. Additional work with unified protocols for determination of metals both in soils and plants (Reeves and Kruckeberg 2018) should help in understanding if there are differences in metal availability in soils of circumboreal regions compared to those of more southern regions.
In conclusion, we stress three possible reasons for the lack of high levels of diversity and endemism in the ultramafic flora in the Circumboreal region and the reduced levels of metal hyperaccumulation observed among the region’s plants: (1) the brief growth period post glaciation (< 12,000 years) has not been adequate for the evolution of full-fledged species obligately endemic to ultramafic soils, (2) water stress and other stressors, including herbivory, hypothesized to drive the evolution of hyperaccumulation, are not as severe compared to those of more warmer climates, (3) low concentration of total/bioavailable metals in soils due to reduced weathering of parent material due to climatic factors and the time available for soil formation due to recent glaciation. These factors may act separately or in concert, leading to the distinct patterns of plant diversity and metal accumulation so far documented on ultramafic soils of the circumboreal region.
References
Adams J (2007) Vegetation–climate interaction. How vegetation makes the global environment. Praxis Publishing Ltd, Chichester
Alekseeva-Popova NV (1970) Elemental chemical composition of plants of the Polar Urals, growing on different rocks. Bot Z 55:1304–1315 (In Russian)
Alekseeva-Popova NV, Drozdova IV (1996) The features of the mineral plant and soil composition on ultrabasic rocks in the Ust-Belskiy massif (the middle reaches of Anadyr river). II. The plants. Bot Z 81:70–78 (In Russian)
Alekseeva-Popova NV, Drozdova IV (2013) Micronutrient composition of plants in the polar urals under contrasting geochemical conditions. Russ J Ecol 44:100–107
Alekseeva-Popova NV, Igoshina TI, Drosdova IV (1995) Metal distribution in the Arctic ecosystems of the Chukotka Peninsula, Russia. Sci Total Environ 160(161):643–652
Alekseeva-Popova NV, Drozdova IV, Kalimova IB (2015) Accumulation of heavy metals by North Caucasian plant species of the Cruciferae family in regards to phytoremediation. Geochem Int 53:456–463
Alexander EB (2004) Varieties of ultramafic soil formation, plant cover, and productivity. In: Boyd RS, Baker AJM, Proctor J (eds) Ultramafic rocks: their soils, vegetation, and fauna. Science Reviews, St. Albans
Alexander EB, Coleman RG, Keeler-Wolf T, Harrison S (2007) Serpentine geoecology of Western North America. Oxford University Press, New York
Al-Shehbaz IA (2014) A synopsis of the genus Noccaea (Coluteocarpeae, Brassicaceae). Harv Pap Bot 19:25–51
Anacker BL (2011) Phylogenetic patterns of endemism and diversity. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley, pp 49–70
Armbruster WS (2014) Multiple origins of serpentine-soil endemism explained by preexisting tolerance of open habitats. PNAS 111:14968–14969
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy Metal Tolerance in Plants: Evolutionary aspects. CRC Press, Boca Raton, pp 155–177
Baker AJM, Proctor J, Reeves RD (1992) The vegetation of ultramafic (Serpentine Soils). In: Proceedings of first international conference on serpentine ecology (19–22 June 1991, Davis, California). Intercept, Andover
Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot Serbica 34:3–14
Bani A, Imeri A, Echevarria G, Pavlova D, Reeves RD, Morel JL, Sulçe S (2013) Nickel hyperaccumulation in serpentine flora of Albania. Fresenius Environ Bull 22:1792–1801
Berazaín R, de la Fuente V, Sánchez-Mata D, Rufo L, Rodríguez N, Amils R (2007) Nickel localization on tissues of hyperaccumulator species of Phyllanthus L. (Euphorbiaceae) from ultramafic areas of Cuba. Biol Trace Element Res 115(1):67–86
Blečić V, Tatić B, Krasnići F (1969) Tri endemične zajednice na serpentinskoj podlozi u Srbiji. Acta Bot Croat 28:43–47
Borhidi A (1992) The serpentine flora and vegetation of Cuba. In: Baker AJM, Proctor J, Reeves RD (eds) The Vegetation of Ultramafic (Serpentine) Soils. In: Proceedings 1st international conference on serpentine ecology. Intercept Ltd., Andover, Hampshire, UK, pp 83–95
Boufford DE, Kartesz JT, Shi S, Zhou R (2014) Packera serpenticola (Asteraceae; Senecioneae), a new species from North Carolina, USA. Syst Bot 39:1027–1030
Boyd R (1998) Hyperaccumulation as a plant defensive strategy. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals, CAB Internetional, Wallingford, pp 181–202
Boyd RS (2012) Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195:88–95. https://doi.org/10.1016/j.plantsci.2012.06.012
Boyd RS (2014) Ecology and evolution of metal-hyperaccumulating plants. In: Rajakaruna N, Boyd R, Harris T (eds) Plant ecology and evolution in harsh environment. Nova Science publishers Inc., New York, pp 227–241
Brady KU, Kruckeberg AR, Bradshaw HDJ (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266
Brearley FQ (2018) Geo-ecological studies on two ultramafic sites in western Ireland. Ecol Res. https://doi.org/10.1007/s11284-018-1584-2
Brooks RR (1983) Biological methods of prospecting for minerals. Wiley, New York
Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Croom Helm, Dioscorides Press, London
Brooks RR (1998) Plants that hyperaccumulate heavy metals. CAB International, Wallingford
Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc Royal Soc Lond B 200:217–224
Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc R Soc Lond Ser B Biol Sci 203:87–403
Brummitt RK, Kent DH, Lusby PS, Palmer RC (1987) The history and nomenclature of Thomas Edmonston’s endemic Shetland Cerastium. Watsonia 16:291–297
Brysting AK (2008) The arctic mouse-ear in Scotland—and why it is not arctic. Plant Ecol Divers 1:321–327
Burgess J, Szlavecz K, Rajakaruna N, Swan C (2015) Ecotypic differentiation of mid-Atlantic Quercus species in response to ultramafic soils. Aust J Bot 63:308–323
Cacho NI, Strauss SY (2014) Occupation of bare habitats, an evolutionary precursor to soil specialization in plants. Proc Nat Acad Sci USA 111:15132–15137
Carter SP, Proctor J, Slingsby DR (1987) Soil and vegetation of the Keen of Hamar serpentine, Shetland. J Ecol 75:21–42
Cecchi L, Selvi F (2009) Phylogenetic relationships of the monotypic genera Halacsya and Paramoltkia and the origins of serpentine adaptation in circum mediterranean Lithospermeae (Boraginaceae): insights from ITS and matK DNA sequences. Taxon 58:700–714
Chytrý M (2012) Vegetation of the Czech Republic: diversity, ecology, history and dynamics. Preslia 84:427–504
Chytrý M, Tichý L (2003) Diagnostic, constant and dominant species of vegetation classes and alliances of the Czech Republic: a statistical revision. Masaryk University Brno, Czech Republic
Cody WJ (1983) Adiantum pedatum ssp. calderi, a new subspecies in Northeastern North America. Rhodora 85:93–96
Coombe DE, Frost LC (1956a) The heaths of the Cornish serpentine. J Ecol 44:226–256
Coombe DE, Frost LC (1956b) The nature and origin of the soils over the Cornish serpentine. J Ecol 44:605–615
Dahl E (1998) The phytogeography of Northern Europe (British Isles, Fennoscandia and adjacent areas). Cambridge University Press, New York
Dennes GE (1845) Proceedings of the botanical society of London. Phytolog 2:95–96
Doksopulo EP (1961) Nickel in rocks, soils, water and plants adjacent to the talc deposits of the Chorchanskaya group. Izdatelstvo Tbiliskogo Universiteta, Tbilisi
Dostál J (1984) Notes to the nomenclature of the taxa of the Czechoslovac flora. Folia Mus Rer Natur Bohem Occid, Bot, Plzeň 21:1–22
Drozdova IV, Alekseeva-Popova NV (1999) Features of plant and soil mineral composition on ultrabasic rocks in the Ust-Belsky massif (the middle reaches of Anadyr river). III. Plants of family Poaceae, Cyperaceae, Ericaceae. Bot Z 84:1–12 (In Russian)
Drozdova IV, Yurtzev BA (1995) Comparative characteristic of plant mineral composition in different ecological plant groups on serpentinites of Southern Chukotka. Bot Z 80:51–59 (In Russian)
Drozdova IV, Alekseeva-Popova NV, Kalimova IB, Belyaeva AI (2013) Accumulation of heavy metals by some species of Brassicaceae fam. in the North Caucasus. Rastytelnye Resursy 49:370–379 (In Russian)
Dvořáková M (1988) Minuartia smejkalii, eine neue Art aus der Minuartia gerardii—Gruppe (Caryophyllaceae). Preslia 60:1–9
Ernst WHO (1987) Population differentiation in grassland vegetation. In: Van Andel J, Bakker JP, Snaydon RW (eds) Disturbance in grasslands. W. Junk, Dordrecht, pp 213–228
Fischer M, Veljović V, Tatić B (1984) Veronica scardica—a neglected species of the Serbian flora. Glasn Inst Za Bot i Bot Baste Univo u Beogradu 13:37–53
Flinn KM, Mikes JL, Kuhns AD (2017) Plant diversity and community composition in eastern North American serpentine barrens. J Torrey Bot Soc 144:125–138. https://doi.org/10.3159/TORREY-D-16-00030
Galey ML, van der Ent A, Iqbal MCM, Rajakaruna N (2017) Serpentine geoecology of South and Southeast Asia. Bot Stud 58:1–28. https://doi.org/10.1186/s40529-017-0167-9
Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. Brassicaceae: characterization, functional genomics and health benefits. Nova Science Publishers Inc, New York, pp 121–148
García-Gonzalez A, Clark SC (1989) The distribution of Minuartia verna and Thlaspi alpestre in the British Isles in relation to 13 soil metals. Vegetatio 84:87–98
Gawler SC (1983) Note on Adiantum pedatum L. ssp. calderi Cody. Rhodora 85:389–390
Ghaderian SM, Mohtadi A, Rahiminejad R, Reeves RD, Baker AJM (2007a) Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant Soil 293:91–97
Ghaderian SM, Mohtadi A, Rahiminejad MR, Baker AJM (2007b) Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environ Pollut 145:293–298
Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna N (2014) A preliminary study of the role of nickel in enhancing flowering of the nickel hyperaccumulating plant Alyssum inflatum Nyár. (Brassicaceae). S Afr J Bot 92:47–52
Gustafson DJ, Romano G, Latham RE, Morton JK (2003) Amplified fragment length polymorphism analysis of genetic relationships among the serpentine barrens endemic Cerastium velutinum Rafinesque var. villosissimum Pennell (Caryophyllaceae) and closely related Cerastium species. J Torrey Bot Soc 130:218–223
Harris T, Rajakaruna N (2009) Adiantum viridimontanum, Aspidotis densa, Minuartia marcescens, and Symphyotrichum rhiannon: additional serpentine endemics from eastern North America. Northeastern Nat sp5:111–120
Harris TB, Olday FC, Rajakaruna N (2007) Lichens of Pine Hill, a peridotite outcrop in eastern North America. Rhodora 109:430–447
Harrison SP, Rajakaruna N (eds) (2011) Serpentine: the evolution and ecology of a model system. Univiversity of California Press, Berkeley
Hughes R, Bachmann K, Smirnoff N, Macnair MR (2001) The role of drought tolerance in serpentine tolerance in the Mimulus guttatus Fischer ex DC. Complex. S Afr J Sci 97:81–586
Igoshina KN (1966) Specific features of the flora and vegetation on hyperbasites of the Polar Urals: the example of Mt Rai-Iz. Bot Z 51:322–338 (In Russian)
Jaffré T (1992) Floristic and ecological diversity of the vegetation on ultramafic rocks in New Caledonia. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic soils, Intercept Ltd, Andover, Hampshire, UK, pp 101–107
Janišová M, Barth AS, Kiehl K, Dengler J (2011) Advances in the conservation of dry grasslands: introduction to contributions from the seventh European Dry Grassland Meeting. Plant Biosyst 145:507–513
Jovanović B, Lakušić R, Rizovški R, Trinajstić I, Zupančić M (eds) (1986) Prodromus phytocenosum Yugoslaviae ad mappam vegetationis 1:2,00,000. Scientific Council of the Vegetation Maps of Yugoslavia, Bribir—Ilok
Jovanović S, Stevanović V, Jovanović-Dunjic R (1992) Contribution to the knowledge on the serpentine vegetation of Serbia. Bull Nat Hist Mus Belgrade 47:43–51
Kabaš E, Alegro A, Kuzmanović N, Jakovljević K, Vukojičić S, Lakušić D (2013) Stipetum novakii ass. nova—a new association of serpentine rocky grassland vegetation (Halacsyetalia sendtneri). Serb Acta Bot Croat 72:169–184
Kaplan Z (1998) Relict serpentine populations of Knautia arvensis s.l. (Dipsacaceae) in the Czech Republic and an adjacent area of Germany. Preslia 70:21–31
Kataeva MN (2013) Availability of elements in tundra soils on acidic and ultramafic rocks in the Polar Urals. Eurasian Soil Sci 46:158–167
Kawase D, Hayashi K, Takeuchi Y, Yumoto T (2010) Population genetic structure of Lilium japonicum and serpentine plant L. japonicum var. abeanum by using developed microsatellite markers. Plant Biosyst 144:29–37
Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508
Kholod SS (2007) Altitudinal and entopic distribution of vascular plants on ultramafic rocks of the Polar Ural. Bot Z 92:289–1319 (In Russian)
Kinzel H (1982) Pflanzenökologie and Mineralstoffwechsel. Ulmer, Stuttgart, p 534
Kitamura S, Momotani Y (1952) Serpentine flora of Island Sugashima, Prov. Shima, Japan. J Phytogeogr Taxon 14:118–119 (In Japanese)
Knjasev MS (2011) Notes on some species of Brassicaceae in Urals and adjacent territories. Novosti Sist Vyssh Rast 42:143–145 (In Russian)
Kolář F, Fér T, Štech M et al (2012) Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid–tetraploid complex of Knautia arvensis (Dipsacaceae). PLoS One 7(7):e39988. https://doi.org/10.1371/journal.pone.0039988
Kolář F, Kaplan Z, Suda J, Štech M (2015) Populations of Knautia in ecologically distinct refugia on the Hercynian massif belong to two endemic species. Preslia 87:363–386
Kotilanen MJ, Salmi V (1950) Two serpentinicolous forms of Cerastium vulgatum L. in Finland. Ann Bot Soc Zool Bot Fenn Vanamo 5:64–69
Krasniqi E, Millaku F, Rexhepi F, Abdullai K (2008) Flora dhe vegjetacioni në terrenet serpentine të malit drenicë. In: Proceedings international conference on biological and environmental sciences, University of Tirana, Faculty of Natural Sciences, Tiranë
Kruckeberg AR (1984) California serpentines: flora, vegetation, geology, soils, and management problems. Univ of California Press, Berkeley
Kruckeberg AR (1986) An essay: the stimulus of unusual geologies for plant speciation. Syst Bot 11:455–463
Kruckeberg AR (1992) Plant life of western North American ultramafics. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks: a world view. Kluwer Academic Publishers, Dordrecht, pp 31–73
Kruckeberg AR (2002) Geology and plant life: the effects of landforms and rock types on plants. University of Washington Press, Seattle
Kulikov PV, Kirsanova OF (2012) Vascular plants reserve “Denezhkin Kamen” (annotated list). In: Novikov VS et al (eds) Flora and fauna reserves. Izdatelstvo komissii RAN, Moscow, pp 1–139 (In Russian)
Kulikov PV, Zolotareva NV, Podgaevskaya EN (2013) Endemic species of the Urals in the flora of Sverdlovsk region. Yekaterinburg, Goshchitskii (In Russian)
Lakušić D, Sabovljević M (2005) Phytocoenological classification of vegetation. In: Lakušić D (ed) Habitats in Serbia, results of the project “Harmonization of national nomenclature in the classification of habitats with the international standards”
Lewis GJ, Bradfield GE (2003) A floristic and ecological analysis at the Tulameen ultramafic (serpentine) complex, Southern British Columbia, Canada. Davidsonia 14:121–128
Lewis GJ, Bradfield GE (2004) Plant community-soil relationships at an ultramafic site in southern British Columbia, Canada. In: Boyd RS, Baker AJM, Proctor J (eds) Ultramafic rocks: their soils, vegetation, and fauna. Science Reviews, St. Albans, pp 191–197
Lewis GJ, Ingram JM, Bradfield GE (2004) Diversity and habitat relationships of bryophytes at an ultramafic site in southern British Columbia, Canada. In: Boyd RS, Baker AJM, Proctor J (eds) Ultramafic rocks: their soils, vegetation, and fauna. Science Reviews, St. Albans, pp 199–204
Malyshev LI (1972) Floristic spectra of Soviet Union. In: Chrshanovsky G, Lavrenko EM, Linczevsky IA (eds) The history of flora and vegetation of Eurasia. Nauka, Leningrad, pp 17–40 (In Russian)
Marin PD, Tatić B (2001) Serpentine soil and plant diversity, with emphasis on the Balkan Peninsula. Bocconea 13:145–150
Marsili S, Roccotiello E, Rellini I, Giordani P, Barberis G, Mariotti MG (2009) Ecological Studies on the Serpentine Endemic Plant Cerastium utriense Barberis. In: Soil and biota of serpentine: a world view. Northeastern Nat sp5:405–421
Martens SN, Boyd RS (2002) The defensive role of Ni hyperaccumulation by plants: a field experiment. Am J Bot 89:998–1003
Mayer E, Greuter W (1985) Aristolochia merxmuelleri, ein neue Serpentin—Endemit aus Sudwest. Serbien Bot Jahr Syst 107:321–327
Mengoni A, Baker AJM, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbrielli R, Gonnelli C (2003) Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by its nrDNA analysis. New Phytol 159:691–699
Millaku F, Krasniqi E, Rexhepi R (2011) The association Stipeto-Convolvuletum compacti ass. nova in Kosovo. Hacquetia 10:137–147
Mizuno T, Nosaka S (1992) The distribution and extent of serpentinized areas in Japan. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks. Kluwer Academic Publishers, Dordrecht, pp 271–311
Mizuno T, Horie K, Nosaka S, Obata H, Mizuno N (2009) Serpentine plants in Hokkaido and their chemical characteristics. Northeast Nat sp5:65–80
Morton JK (2004) Cerastium velutinum Rafinesque var. villossissimum (Pennell) J. K. Morton. Sida 21:887
Nagy L, Proctor J (1997) Plant growth and reproduction on a toxic alpine ultramafic soil: adaptation to nutrient limitation. New Phytolog 137:267–274
Niketić M (1994) Cerastium neoscardicum, a new species of ser. Alpina from Mt Shar-planina, Serbia. Bull Inst Bot Bot Gard Univ Belgrade Belgrade Yugosl 26–27:63–70
Novák F (1927) Ad florae Serbiae cognitionem additamentum alterum. Preslia 5:65–137
Novák F (1928) Quelques remarques relatives au problème de la vértétation sur les terrains serpentiniques. Preslia 6:42–71
Nyberg Berglund AB, Westerbergh A (2001) Two postglacial immigration lineages of the polyploid Cerastium alpinum (Caryophyllaceae). Hereditas 134:171–183
Nyberg Berglund AB, Saura A, Westerbergh A (2001) Genetic differentiation of a polyploid plant on ultramafic soils in Fennoscandia. S Afr J Sci 97:533–535
Nyberg Berglund AB, Dahlgren S, Westerbergh A (2004) Evidence for parallel evolution and site-specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytol 161:199–209
O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In: Harrison SP, Rajakaruna N (eds) Serpentine: the evolution and ecology of a model system Berkeley. University of California Press, Berkeley, pp 97–137
Paris CA (1991) Adiantum viridimontanum, a new maidenhair fern in Eastern North America. Rhodora 93:105–121
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644
Pichi-Sermolli R (1948) Flora e vegetazione delle serpentine e delle altre ofioliti dell’alta valle del Tevere (Toscana). Webbia 6:1–380
Pope N, Harris TB, Rajakaruna N (2010) Vascular plants of adjacent serpentine and granite outcrops on the Deer Isles, Maine, USA. Rhodora 112:105–141
Proctor J (1992) Chemical and ecological studies on the vegetation of ultramafic sites in Britain. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rockes: a world view. Kluwer Academic Publishers, Dordrecht, pp 135–167
Proctor J (1999) Toxins, nutrient shortages and droughts: the serpentine challenge. Trends Ecol Evol 14:334–335
Proctor J (2003) Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East. Perspect Plant Ecol Evol Syst 6:105–124
Proctor J, Woodell SRJ (1971) The plant ecology of serpentine. 1. Serpentine vegetation of England and Scotland. J Ecol 59:375–395
Proctor J, Woodell SRJ (1975) The ecology of serpentine soils. Adv Ecol Res 9:255–366
Proctor J, Alekseeva-Popova NV, Kataeva MN, Kravkina IM, Yurtsev BA, Drozdova IV (2005) Arctic ultramafics: new investigations on Polar Urals vegetation. In: Proceedings of the IV international congress on ultramafic (serpentine) ecology, London, pp 121–136
Rajakaruna N (2004) The edaphic factor in the origin of plant species. Int Geol Rev 46:471–478
Rajakaruna N (2018) Lessons on evolution from the study of edaphic specialization. Bot Rev. https://doi.org/10.1007/s12229-017-9193-2 (in press)
Rajakaruna N, Boyd RS (2008) The edaphic factor. In: Jørgensen SE, Fath BD (eds) The encyclopedia of ecology, vol 2. Elsevier, Oxford, pp 1201–1207
Rajakaruna N, Harris TB, Alexander EB (2009) Serpentine geoecology of eastern North America: a review. Rhodora 111:21–108
Raymond M (1955) Une variété nouvelle du Cerastium arvense L. Bull de la Société Bot Fr 102:125–127
Reeves RD (1970) Hyperaccumulation of trace elements by plants. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils, Springer, Netherlands, pp 25–52
Reeves RD (1988) Nickel and zinc accumulation by species of Thlaspi L., Cochlearia L. and other genera of the Brassicaceae. Taxon 37:309–318
Reeves RD, Baker AJM (1984) Studies on metal uptake by plants from serpentine and non-serpentine populations of Thlaspi goesingense Hálácsy (Cruciferae). New Phytol 98:191–204
Reeves RD, Baker AJM (2000) Metal accumulating plants. In: Raskin I, Ensley B (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229
Reeves RD, Brooks RR (1983) European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. J Geochem Explor 18:275–283
Reeves RD, Brooks RR, Robert J (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxon 29:629–633
Reeves RD, Brooks RR, Macfarlane RM (1981) Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae). Am J Bot 68:708–712
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel accumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217–224
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38
Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293:107–119
Reeves RD, Kruckeberg AR (2018) Re-examination of the elemental composition of some Caryophyllaceae on North American ultramafic soils. Ecol. Res. https://doi.org/10.1007/s11284-017-1556-y
Ritter-Studnička H (1970) Die vegetation der serpentinvorkommen in Bosnien. Vegetatio 21:75–156
Rivas-Martínez S (1997) Syntaxonomical synopsis of the potential natural plant communities of North America, I (Compendio sintaxonómico de la vegetación natural potencial de Norteamérica, I). Itinera Geobot 10:54–90
Roberts BA, Proctor J (1992) The ecology of areas with serpentinized rocks: a world view. Kluwer Academic Publishers, Dordrecht
Robinson BH, Brooks RR, Kirkman JH, Gregg PEH, Alvarez HV (1997) Edaphic influences on a New Zealand ultramafic (“serpentine”) flora: a statistical approach. Plant Soil 188:11–20
Rodríguez-Rojo MP, Sánchez-Mata D, Rivas-Martínez S, Barbour MG (2001a) Syntaxonomical approach for classification of the Californian serpentine annual grasslands. Lazaroa 22:83–94
Rodríguez-Rojo MP, Sánchez-Mata D, Gavilán RG, Rivas-Martínez S, Barbour MG (2001b) Typology and ecology of the Californian serpentine annual grasslands. J Veg Sci 12:687–698
Rune O (1953) Plant life on serpentine and related rocks in northern Sweden. Acta Phytogeogr Suecica 31:1–139
Rune O (1954) Notes on the flora of the Gaspé Peninsula. Svensk Bot Tidskr 48:117–138
Rune O, Westerberg A (1992) Phytogeographic aspects of the serpentine flora of Scandinavia. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 469–494
Safford HD, Viers JH, Harrison SP (2005) Serpentine endemism in the California flora: a database of serpentine affinity. Madroňo 52:222–257
Sakaguchi S, Horie K, Kimura T et al (2017) Phylogeographic testing of alternative histories of single-origin versus parallel evolution of early flowering serpentine populations of Picris hieracioides L. (Asteraceae) in Japan. Ecol Res. https://doi.org/10.1007/s11284-017-1536-2
Sánchez-Mata D, Rodríguez-Rojo MP (2016) Mediterranean ultramafic (serpentine) chaparrals of California (USA): a geobotanical overview. In: Box EO (ed) Vegetation structure and function at multiple spatial, temporal and conceptual scales. Geobotany Studies. Springer, Berlin, pp 285–312
Sánchez-Mata D, Rodríguez-Rojo MP, Barbour MG (2004) California ultramafic vegetation: biodiversity and phytosociological survey. In: Boyd R et al (eds) Actas de la IV Conferencia Internacional sobre Ecología de Serpentina. Science Reviews, La Habana, pp 177–181
Sánchez-Mata D, de la Fuente V, Rufo L, Rodríguez N, Amils R (2013) Streptanthus purpureus sp. nova (Cruciferae), an endemic nickel hyperaccumulator from Sierra Nevada (California, USA). Lazaroa 34:275–283
Scott W, Palmer R (1987) The flowering plants and ferns of the Shetland Islands. The Shetland Times Ltd, Lerwick
Severne BC, Brooks RR (1972) A nickel accumulating plant from Western Australia. Planta 103:91–94
Shallari S, Schwartz C, Hasko A, Morel JL (1998) Heavy metals in soils and plants of serpentine and industrial sites of Albania. Sci Tot Environ 209:133–142
Shewry PR, Peterson PJ (1976) Distribution of chromium and nickel in plants and soil from serpentine and other sites. J Ecol 64:195–212
Sirois L, Grandtner MM (1992) A phyto-ecological investigation of the Mount Albert serpentine plateau. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks: a world view. Kluwer Academic Publishers, Dordrecht, pp 115–133
Skinner MW, Pavlik BM (1994) California Native Plant Society’s inventory of rare and endangered plants of California. California Native Plant Society Special Publication Number 1, Sacramento
Sleep A (1985) Speciation in relation to edaphic factors in the Asplenium adiantum-nigrum group. Proc R Soc Edinb 86:325–334
Spence DHN (1957) Studies on the vegetation of Shetland. I. The serpentine debris vegetation in Unst. J Ecol 45:917–945
Spence DHN (1958) The flora of Unst, Shetland, in relation to geology. Trans Bot Soc Edinb 37:163–173
Spence DHN (1959) Studies on the vegetation of Shetland. II. Reasons for the restriction of exclusive pioneers to serpentine debris. J Ecol 47:641–649
Spence DHN (1970) Scottish serpentine vegetation. Oikos 21:22–31
Spence DHN, Millar EA (1963) An experimental study of the infertility of Shetland serpentine soil. J Ecol 51:333–343
Stace CA (1997) New flora of the British Isles. Cambridge University Press, Cambridge
Stamenković M, Andrejić G, Mihailović N, Šinžar-Sekulić J (2017) Hyperaccumulation of Ni by Alyssum murale Waldst. and Kit. from ultramafics in Bosnia and Herzegovina. Appl Ecol Environ Res 15:359–372
Stebbins GL (1984) Polyploidy and the distribution of the arctic-alpine flora: new evidence and a new approach. Bot Helv 94:1–13
Steele B (1955) Soil pH and base status as factors in the distribution of calcicoles. J Ecol 43:120–132
Štěpánek J (1989) Chrastavec rolní krkonošský—Knautia arvensis (L.) Coulter subsp. pseudolongifolia (Szabó) O. Schwarz. In: Slavík B et al (eds) Studie ČSAV 10: Vybrané ohrožené druhy flóry ČSR. Academia, Praha, pp 25–36
Stevanović V, Tan K, Iatrou G (2003) Distribution of the endemic Balkan flora on serpentine I: obligate serpentine endemics. Plant Syst Evol 242:149–170
Takhtajan AL (1986) Floristic regions of the world. University of California Press, Berkeley
Tan K, Gjeta E, Mullaj A, Shuka L, Vold G (2013) On the identity of Anchusa leucantha (Boraginaceae) from northern Greece. Phytotaxa 140:35–42
Tatić B, Krivošej Z (1997) Tulipa serbica (Liliaceae), a new species from Serbia. Bocconea 5:733–736
Tatić B, Veljović V (1992) Distribution of serpentinized massifes on the Balkan peninsulas and their ecology. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks. A world view. Kluwer Academic Publishers, Dordrecht, pp 199–215
Teptina AY, Paukov AG (2012) Petrophytic plants—accumualtors of heavy metals on the ultramafic rocks of the Urals. In: Mukhin VA (ed) Biological diversity of the plant world of the urals and adjacent territories. Goshchitskii, Yekaterinburg, pp 137–138 (In Russian)
Teptina AY, Paukov AG (2015) Nickel accumulation by species of Alyssum and Noccaea (Brassicaceae) from ultramafic soils in the Urals, Russia. Aust J Bot 62:78–84
Teptina AY, Lebedeva MV, Yamalov SM (2018) Some petrophytic steppe communities of the Middle Urals. Veg Russ 32 (in press, in Russian)
Tomimatsu H, Hoya A, Takahashi H, Ohara M (2004) Genetic diversity and multilocus genetic structure in the relictual endemic herb Japonolirion osense (Petrosaviaceae). J Plant Res 117:13–18
Tomović G, Mihailović N, Tumi A, Gajić B, Mišljenović T, Niketić M (2013) Trace metals in soils and several Brassicaceae plant species from serpentine sites of Serbia. Arch Environ Prot 39:29–49
Tomović G, Niketić M, Lakušić D, Ranđelović V, Stevanović V (2014) Balkan endemic plants in Central Serbia and Kosovo regions: distribution patterns, ecological characteristics, and centres of diversity. Bot J Linn Soc 176:173–202
Tumi AF (2013) Bioaccumulation potential of selected plant species of the family Brassicaceae from serpentine habitats in Serbia. Doctoral Dissertation. Belgrade
Tyndall RW, Hull DJC (1999) Vegetation, flora, and plant physiological ecology of serpentine barrens of eastern North America. In: Anderson RC, Fralish JS, Baskin JM (eds) Savannas, barrens, and rock outcrop plant communities of North America. Cambridge University Press, New York, pp 67–82
Tzonev R, Pavlova D, Sánchez-Mata D, de la Fuente V (2013) Contribution to the knowledge of Bulgarian serpentine grasslands an their relationships with Balkan serpentine taxa. Plant Biosyst 147:955–969
Van der Ent A, Jaffré T, L’Huillier L, Gibson N, Reeves RD (2015) The flora of ultramafic soils in the Australia-Pacific Region: state of knowledge and research priorities. Aust J Bot 63:173–190
Vasié O, Diklié N (2001) The flora and vegetation on serpentinites in Serbia—a review. Bocconea 13:151–164
Vassilev K, Pedashenko H, Nikolov SC, Apostolova I, Dengler J (2011) Effect of land abandonment on the vegetation of upland semi-natural grasslands in the Western Balkan Mts., Bulgaria. Plant Biosyst 145:654–665
Verger J-P (1992) Vegetation and soils in the Valle d’Aosta (Italy). In: Baker AJM, Proctor J, Reeves RD (eds) Vegetation of ultramafic (Serpentine) soils. Intercept, Hampshire, pp 175–195
Vicherek J (1970) Ein Beitrag zur Syntaxonomie der Felsspalten- und Rissenpflanzengesellschaften auf Serpentin in Mitteleuropa. Folia Fac Sci Nat Univ Purkynianae Brun Biol 26:83–89
Vit P, Wolfova K, Urfus T, Tajek P, Suda J (2014) Interspecific hybridization between rare and common plant congenersinferred from genome size data: assessing the threat to the Czech serpentine endemic Cerastium alsinifolium. Preslia 86:95–117
Watson HC (1860) Part first of a supplement to the Cybele Britannica. London
Yurtsev BA, Alekseeva-Popova NV, Kataeva MN (2001) Species diversity of local floras of the Polar Urals under contrasting geochemical conditions. In: Veselov AE (ed) Biodiversity in Northern Europe: Abstract International Conference, Petrozavodsk, pp 204–205
Yurtzev BA, Alexeeva-Popova NV, Drozdova IV, Kataeva MN (2004) Characteristics of Vegetation and Soils of Polar Urals under Geochemical Conditions: 1. Calciphyte and Acidophyte Communities. Bot Z 89:28–41 (In Russian)
Acknowledgements
The authors wish to thank the two anonymous reviewers for their useful comments on the manuscript. The work of AT and AP is financially supported by RFBR (Grant 16-04-01346) and the Ministry of Education and Science of the Russian Federation Agreement no. 02.A03.21.0006.
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Teptina, A., Paukov, A. & Rajakaruna, N. Ultramafic vegetation and soils in the circumboreal region of the Northern Hemisphere. Ecol Res 33, 609–628 (2018). https://doi.org/10.1007/s11284-018-1577-1
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DOI: https://doi.org/10.1007/s11284-018-1577-1