Article

The genus Odontarrhena (Brassicaceae) in Albania: Taxonomy and Nickel accumulation in a critical group of metallophytes from a major serpentine hot-spot

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

Metal hyperaccumulator plants represent a unique biological resource for scientific research and practical applications. Though essential, however, an adequate knowledge of the systematics of these plants is often missing. This is the case of Odontarrhena, a large but taxonomically critical group of nickel hyperaccumulators from Eurasia. We present a study on this genus in Albania, to fill a gap in our knowledge of this group from a major centre of diversity of metallicolous flora, and to contribute updated information to the Global Hyperaccumulator Database. Morphological and karyological analyses of material from field collections across all major serpentine outcrops in the country, in different years and seasons, allowed to delimit seven taxa: O. albiflora, O. chalcidica, O. moravensis, O. sibirica, O. decipiens, O. smolikana subsp. glabra and O. rigida. The three latter taxa have been long neglected and were resurrected in view of their clear distinctness, while commonly accepted taxa such as O. bertolonii subsp. scutarina and O. markgrafii were reduced to synonymy of O. chalcidica due to the lack of consistent differentiation. Polyploidy was prevalent, while diploid complements were typical of the two vicariant endemics O. rigida and O. moravensis. Types are indicated or newly designated for each entity, and nomenclatural issues are addressed based on in-depth studies of literature and herbarium material. Revised descriptions, phenology, habitat and distribution data are given for each taxon, as well as original iconographies and chromosome counts. A revised identification key is provided. Shoot nickel concentrations were determined to assess accumulation levels of taxa and populations in natural conditions and their potential for phytoextraction of this metal from the soil. With ca. 23000 and 17000 µg of Ni g-1 of shoot dry weight, respectively, the tetraploids O. chalcidica and O. decipiens were the most promising candidates, especially the latter for its robust habit.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... While the taxa from Greece are better understood, some of those from Albania, the former Yugoslav Republic of Macedonia (FYROM), and Bulgaria are still poorly known, preventing a correct estimation of the diversity of accumulators in the Balkans to be presented. A recent systematic revision of the genus in Albania (Cecchi et al., 2018) points to the existence of seven taxa, of which six Ni-hyperaccumulators are restricted to ultramafic soils (except for O. chalcidica, facultative serpentinophyte). A polyploid species of likely hybrid origin between O. chalcidica and O. smolikana, originally described from Mt. Smolikas (Greece) as Alyssum decipiens Nyár. ...
Article
Full-text available
Ultramafic soils are typically enriched in nickel (Ni), chromium (Cr), and cobalt (Co) and deficient in essential nutrients, making them unattractive for traditional agriculture. Implementing agromining systems in ultramafic agricultural soils represent an ecological option for the sustainable management and re-valorisation of these low-productivity landscapes. These novel agroecosystems cultivate Ni-hyperaccumulating plants which are able to bioaccumulate this metal in their aerial plant parts; harvested biomass can be incinerated to produce Ni-enriched ash or "bio-ore" from which Ni metal, Ni ecocatalysts or pure Ni salts can be recovered. Nickel hyperaccumulation has been documented in ∼450 species, and in temperate latitudes these mainly belong to the family Brassicaceae and particularly to the genus Odontarrhena (syn. Alyssum pro parte). Agromining allows for sustainable metal recovery without causing the environmental impacts associated with conventional mining activities, and at the same time, can improve soil fertility and quality and provide essential ecosystem services. Parallel reductions in Ni phytotoxicity over time would also permit cultivation of conventional agricultural crops. Field studies in Europe have been restricted to Mediterranean areas and these only evaluated the Ni-hyperaccumulator Odontarrhena muralis s.l. Two recent EU projects (Agronickel and LIFE-Agromine) have established a network of agromining field sites in ultramafic regions with different edapho-climatic characteristics across Albania, Austria, Greece and Spain. Soil and crop management practices are being developed so as to Kidd et al. Sustainable Agromining Systems for Nickel Recovery optimize the Ni agromining process; field studies are evaluating the potential benefits of fertilization regimes, crop selection and cropping patterns, and bioaugmentation with plant-associated microorganisms. Hydrometallurgical processes are being up-scaled to produce nickel compounds and energy from hyperaccumulator biomass. Exploratory techno-economic assessment of Ni metal recovery by pyrometallurgical conversion of O. muralis s.l. shows promising results under the condition that heat released during incineration can be valorized in the vicinity of the processing facility.
Article
Full-text available
Odontarrhena bertolonii is an endemic serpentine species of Tuscany and Liguria and a model system for nickel-hyperaccumulation research in plants. Phenotypic, genetic and karyological variability between populations was previously detected, but existence and distribution of cytotypes was unknown. Accordingly, we examined ploidy level in eight populations from the species range and tested the polyploid fitness hypothesis by analysing relationships with plant phenotype and seed germination capacity. Accessions from central-western Tuscany and Liguria resulted diploid, while those from the upper Tiber valley were tetraploid. Autopolyploidy via unreduced gametes is likely the mechanism for the origin of tetraploid plants. Size and mass were higher in tetraploid seeds, which germinated faster and to higher percentages than diploid ones. Tetraploid plants were more robust and taller, with more richly branched inflorescences. Silicle shape and size did not differ, but style was longer in tetraploids and seeds had a larger wing. Overall, these results supported a higher fitness in polyploids. Multivariate analysis showed continuous variation but consistent differentiation between diploid and tetraploid accessions. Taxonomically, the tetraploid populations at the eastern limit of the species range in the upper Tiber valley can be referred to a new subspecies, here described as O. bertolonii subsp. cesalpina.
Article
Full-text available
Aims Nickel hyperaccumulator plants require highly evolved mechanisms to avoid cellular-level toxicity to cope with the high prevailing concentrations of nickel in their seeds and seedlings. This study aimed to investigate tissue distribution and dynamics of Ni and other physiologically relevant elements during the germination of hyperaccumulators. Methods Berkheya coddii Roessler (Asteraceae) and Odontarrhena muralis (Waldst. & Kit.) Endl., formerly Alyssum murale (Waldst. & Kit.) (Brassicaceae), were germinated for several days at room temperature before using synchrotron micro X-ray Fluorescence Spectroscopy (µXRF) to obtain high-sensitivity and high-resolution images of live/hydrated plants at various stages of seed germination and seedling growth. Results The results show that fruits and seeds of both species were highly enriched in nickel. In Berkheya coddii, nickel was located in the cotyledons, the micropylar area, the seed coat, and the point of attachment of the pappus cypselae. In Odontarrhena muralis seeds, nickel occurred in the cotyledons and hypocotyl. The emergence of true leaves initiates nickel and calcium redistribution within seedlings in both species. Conclusions The diversity in physiological responses to nickel in Berkheya coddii and Odontarrhena muralis does not only occur at the mature stage but is inherent to both species as seed elemental storage and tolerance mechanisms during seedling development differ.
Article
Full-text available
Background Nickel (Ni) phytomining operations cultivate hyperaccumulator plants (‘metal crops’) on Ni-rich (ultramafic) soils, followed by harvesting and incineration of the biomass to produce a high-grade ‘bio-ore’ from which Ni metal or pure Ni salts are recovered. Scope This review examines the current status, progress and challenges in the development of Ni phytomining agronomy since the first field trial over two decades ago. To date, the agronomy of less than 10 species has been tested, while most research focussed on Alyssum murale and A. corsicum. Nickel phytomining trials have so far been undertaken in Albania, Canada, France, Italy, New Zealand, Spain and USA using ultramafic or Ni-contaminated soils with 0.05–1 % total Ni. Conclusions N, P and K fertilisation significantly increases the biomass of Ni hyperaccumulator plants, and causes negligible dilution in shoot Ni concentration. Organic matter additions have pronounced positive effects on the biomass of Ni hyperaccumulator plants, but may reduce shoot Ni concentration. Soil pH adjustments, S additions, N fertilisation, and bacterial inoculation generally increase Ni phytoavailability, and consequently, Ni yield in ‘metal crops’. Calcium soil amendments are necessary because substantial amounts of Ca are removed through the harvesting of ‘bio-ore’. Organic amendments generally improve the physical properties of ultramafic soil, and soil moisture has a pronounced positive effect on Ni yield. Repeated ‘metal crop’ harvesting depletes soil phytoavailable Ni, but also promotes transfer of non-labile soil Ni to phytoavailable forms. Traditional chemical soil extractants used to estimate phytoavailability of trace elements are of limited use to predict Ni phytoavailability to ‘metal crop’ species and hence Ni uptake.
Article
Full-text available
Previous molecular phylogenetic studies have contributed greatly to our knowledge about the phylogenetic position and infra-generic relationships of the genus Alyssum. Nevertheless, due to limited sampling and incongruences between the different markers used, the phylogenetic relationships within the genus are still unresolved. In this study, the phylogenetic relationships within Alyssum were studied using nrDNA ITS and plastid trnL-F sequences from 171 accessions representing 112 species from five sections of the genus. The phylogenetic analyses confirmed the paraphyly and recognition of two main clades in the genus. The first clade included the sections Alyssum, Gamosepalum and most species from sect. Psilonema. Alyssum lanigerum from sect. Odontarrhena was inferred to be nested in this clade only by the ITS dataset. The other clade contained the sections Meniocus, Odontarrhena and the genus Clypeola. The monophyly of the five sections defined by morphology was not well supported by molecular data. Species of the sections Gamosepalum and Psilonema (apart from A. homalocarpum) were intermixed with species of sect. Alyssum, and the monophyly of sect. Meniocus and the genus Clypeola were supported only by the trnL-F dataset. Neither sect. Odontarrhena nor that of its three subsections, subsect. Inflata, Compressa and Samarifera, were recovered as monophyletic. The incongruence between morphology and molecular data indicates that the current taxonomic circumscription of the genus and sections need to be revised.
Article
Full-text available
Database of published chromosome numbers and ploidy-level estimates of the tribe Alysseae is presented, together with the revised generic concept and the list of accepted names, to reflect the most recent taxonomic and phylogenetic studies in Alysseae. It is available on-line at www.alysseae.sav.sk. The tribe encompasses 24 genera and 277 species. Chromosome numbers and/or ploidy levels are known for 171 out of 297 recognized taxa. Of these, 95 (55.6 %) taxa are diploids, 43 (25.1 %) are polyploids, and 33 (19.3 %) involve both diploids and polyploids. The most common base chromosome number in the tribe is x = 8 and less frequent is x = 7. The highest variation in base chromosome numbers (x = 7, 8, 11, 15) is found in the genus Hormathophylla. A key to all genera and descriptions of the two new genera Cuprella and Resetnikia are presented. Many new nomenclatural combinations, mainly in the re-established Odontarrhena (77), are proposed.
Article
Full-text available
Botanical exploration of serpentine soils in Turkey and neighbouring countries has shown that the region includes at least 59 taxa capable of hyperaccumulating nickel (to >0.1% of plant dry weight). These hyperaccumulators belong to the Brassicaceae (Aethionema R.Br., Alyssum L., Bornmuellera Hausskn., Pseudosempervivum (Boiss.) Grossh. (Cochlearia L.), and Thlaspi L. s.l.) and the Asteraceae (Centaurea L.). We review present knowledge of the hyperaccumulators and provide additional data recently obtained. Some species are serpentine-endemic and invariably Ni hyperaccumulating; others show more complex distribution and Ni-accumulating behaviour. Many are good subjects for biochemical studies on the Ni-accumulation and sequestering processes. There is potential in Turkey for exploiting Ni hyperaccumulation for remediation of Ni-contaminated soils ('phytoremediation') and for economical selective extraction of metal compounds by cropping hyperaccumulators ('phytomining'). However, there is a need for further exploration of the natural resources and some further taxonomic work by traditional and DNA methods. Attention must be paid to conservation issues, as some of the relevant species are quite rare.
Chapter
Full-text available
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 microevolutionary 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 selection 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 experimentally 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.
Article
Full-text available
Serpentine soils are widespread in Albania, they host some widespread species and several nickel hyperaccumulating species. The objectives of the study were the identification and collection of new and rare species, the discovery of new instances of Ni hyperaccumulation, in which plant species can accumulate Ni to concentrations exceeding 0.1% of the plant dry weight. In Albania, there has already been special interest in Ni accumulation by Alyssum murale in Pojska (Pogradec). We now report instances of hyperaccumulation of Ni (reaching shoot concentrations of 0.5-1.26% d.w.) in plants of some serpentine soils i.e. in Kukës, Qafë Shtamë, Gramsh and Librazhd. Most plants from these soils showed slightly elevated Ni concentrations in comparison with those from other soil types: about 11-100 mg kg-1, rather than 0.5-10 mg kg-1. In some species Ni content ranged between 145-275 mg kg-1, while the same species from the non-serpentine substrata contained very low Ni concentrations as expected. Full knowledge of Albanian Ni hyperaccumulator plants and their properties is of interest because of their possible use in phytomining. This study was undertaken in the framework of the need for further exploration of the natural resources and the associated conservation issues.
Article
Full-text available
Sequence data from the nuclear ribosomal internal transcribed spacer (ITS) region of 85 species (131 accessions) were used to determine the tribal limits, monophyly status, and phylogenetic intra-tribal relationships of genera within the tribe Alysseae (Brassicaceac). Both maximum parsimony and maximum likelihood analyses support the recognition of the tribe Alysseae s. str. (12 genera: Alyssoides, Alyssum. Aurinia, Berteroa, Bornmuellera, Clastopus, Clypeola, Degenia, Fibigia, Galitzkya, Hormathophylla, and Physoptychis). Six well-supported clades were recognized within the Alysseae clade, including two Alyssum clades (one of which includes Clypeola). an Alyssoides and allies clade (includes Alyssoides. Bornmuellera, Clastopus, Degenia, Fibigia, Hormathophylla, and Physoptychis), a Berteroa and allies clade (includes Aurinia, Berteroa, and Galitzkya), a Bornmuellera clade, and a Hormathophylla clade. Morphological and cytological support for these clades is reviewed. The ITS data support the exclusion of the following taxa from the Alysseae, with appropriate tribal assignment given in parentheses: Alyssum klimesii Al-Shehbaz (Camelineae), Asperuginoides (unresolved), Athysanus (Arabideae), Botschantzevia (Arabideae), Didymophysa (unresolved), Farsetia (Malcolmieae), Lobularia (Malcolmieae), and Ptilotrichum (Arabideae). Farsetia and Lobularia are inferred to be monophyletic, and based on molecular and morphological characters they are assigned to Malcolmieae, a recently described tribe.
Article
Full-text available
New light is shed on the evolutionary affinities and generic diversity in Alysseae (Brassicaceae) by means of nuclear DNA sequences. Internal transcribed spacer analysis was used to assess the relationships and the monophyletic status of Aurinia and Ptilotrichum, when defined to include three poorly known taxa from southeast Europe. The alpine Ptilotrichum rupestre from central Appennines and its Balkan and Anatolian relative Ptilotrichum cyclocarpum clustered together as sister to Bornmuellera and Leptoplax, while their evident lack of affinity with the Asian type species of Ptilotrichum (Arabideae) leads to the definitive exclusion of the latter from the European flora. To accommodate the two species mentioned above, the so far neglected genus Phyllolepidum is accepted. The rare pontic endemic Aurinia uechtritziana resulted closely related to Berteroa and Galitzkya and is treated here as the sole member of Lepidotrichum. Comparative scanning electron micrograph analyses of trichome morphology are consistent with the phylogenetic evidence. The new combinations Phyllolepidum cyclocarpum and P. cyclocarpum subsp. pindicum are proposed, and a key for the identification of all European genera of the Alysseae is presented.
Article
Full-text available
Ultramafic soils are widespread in the Balkans. Albania and Greece are the richest in the number of endemics, including several hyperaccumulator species, growing on serpentine. The objectives of this study were to understand the potential of Ni hyperaccumulation of these species in close relation with the characteristics of their native soil environments. Collection of both plant samples (analysis of element concentrations in aerial parts) and soil samples (analysis of total elements, DTPA-extractable Ni, Fe, and Ni distribution in mineral phases) allowed evaluation of phenotypic efficacy in hyperaccumulating Ni. Nickel availability in soils is controlled by soil weathering and mineral-bearing phases. Unsurprisingly, the highest levels of Ni availability were associated with amorphous Fe-oxides in moderately weathered Cambisols or with high-exchange capacity clays in well-evolved Vertisols. The highest Ni concentrations in leaves were found in Alyssum murale in Pojska (Albania; 2.0%), Alyssum markgrafii in Gjegjan (Albania; 1.9%), Bornmuellera baldacii subsp. markgrafii in Gramsh (Albania; 1.4%), and Leptoplax emarginata in Trigona (Greece; 1.4%). We identified a new member in the Albanian Ni-hyperaccumulator flora: Thlaspi ochroleucum in Pojska (Albania: 0.13% Ni) and in Pishkash (0.14% Ni). With regard to Ni availability in soils, A. markgrafii (Albania) is the most efficient Ni-hyperaccumulator among all species. Alyssum murale, which is widespread in the serpentines of the Balkans, accumulates Ni, with leaf concentration being negatively correlated to total Ca content of soils regardless of Ni availability (DTPA extractable Ni). If this relationship is confirmed, it would mean that genetic variability is not the main factor that explains the hyperaccumulation performance of this species.
Article
Full-text available
Ultramafic outcrops are widespread in Albania and host several Ni hyperaccumulators (e.g., Alyssum murale Waldst. & Kit.). A field experiment was conducted in Pojske (Eastern Albania), a large ultramafic area in which native A. murale was cultivated. The experiment consisted in testing the phytoextraction potential of already installed natural vegetation (including A. murale) on crop fields with or without suitable fertilisation. The area was divided into six 36-m2 plots, three of which were fertilised in April 2005 with (NPK+S). The soil (Magnesic Hypereutric Vertisol) was fully described as well as the mineralogy of horizons and the localisation of Ni bearing phases (TEM-EDX and XRD). Ni availability was also characterised by Isotopic Exchange Kinetics (IEK). The flora was fully described on both fertilised and unfertilised plots and the plant composition (major and trace elements) and biomass (shoots) harvested individually were recorded. The soil had mainly two Ni-bearing phases: high-Mg smectite (1.3% Ni) and serpentine (0.7% Ni), the first one being the source of available Ni. Ni availability was extremely high according to IEK and confirmed by Ni contents in Trifolium nigriscens Viv. reaching 1,442mgkg−1 (A new hyperaccumulator?). Total biomass yields were 6.3tha−1 in fertilised plots and 3.2tha−1 in unfertilised plots with a highly significant effect: fertilisation increased dramatically the proportion of A. murale in the plots (2.6tha−1 vs. 0.2tha−1). Ni content in the shoots of A. murale reached 9,129mgkg−1 but metal concentration was not significantly affected by fertilisation. Phytoextracted Ni in total harvest reached 25kg Niha−1 on the fertilised plots. It was significantly lower in unfertilised plots (3kg Niha−1). Extensive phytomining on such sites could be promising in the Albanian context by domesticating already installed natural populations with fertilisation.
Article
Full-text available
Metal hyperaccumulation is a striking trait exhibited by many plant species, but the evolutionary ecology of metal hyperaccumulation is poorly understood. It has been widely hypothesized that metal hyperaccumulation evolved to protect plants from herbivory. However, there is currently little evidence that metal hyperaccumulation enhances the fitness of plants in the presence of herbivory. In this study, we conducted a multi-factor greenhouse experiment to examine the effects of two soil nickel concentrations (unamended (0μg/g) and nickel amended (600μg/g)), and three levels of artificial damage (0, 10 and 50%) on the growth of plants from two populations of Thlaspi montanum var. montanum. We observed a significant interaction between soil nickel and artificial damage. An a posteriori analysis of this interaction revealed that the presence of nickel significantly improved the ability of T. montanum to tolerate the negative effects of intense damage. Our results indicate that metal hyperaccumulation could benefit T. montanum by increasing its tolerance to damage. This study suggests that there is a potential for the evolution of metal hyperaccumulation in response to intense herbivory on T. montanum.
Article
Full-text available
A NUMBER of terrestrial plants accumulate large quantities of metals such as zinc, manganese, nickel, cobalt and copper in their shoots1. The largest group of these so-called 'metal hyperaccumulators' is found in the genus Alyssum, in which nickel concentrations can reach 3% of leaf dry biomass2,3. Apart from their intrinsic interest, plants exhibiting this trait could be of value in the decontamination of metal-polluted soils4-6. However, the biochemical basis of the capacity for metal accumulation has not been elucidated. Here we report that exposing hyperaccumu-lator species of Alyssum to nickel elicits a large and proportional increase in the levels of free histidine, which is shown to be coordinated with nickel in vivo. Moreover, supplying histidine to a non-accumulating species greatly increases both its nickel tolerance and capacity for nickel transport to the shoot, indicating that enhanced production of histidine is responsible for the nickel hyperaccumulation phenotype in Alyssum.
Article
Full-text available
Experiments were carried out in Italy on the potential use of the hyperaccumulator Alyssum bertolonii in phytomining of ultramafic soils for Ni. In situ experimental plots at Murlo, Tuscany were fertilized with various regimes during a 2-year period. The best fertilizer treatment (N + K + P) gave a threefold increase of the biomass of reproductive matter to 9.0 t/ha without dilution of the unfertilized Ni content. A Ni content of 0.8% in dry matter (11% in ash), would give a Ni yield of 72 kg/ha without need of resowing for a further crop. There was no correlation between the age of a plant and its Ni content. The long-term cropping sustainability of the soils was simulated by sequential extractions with KH phthalate solutions at pH 2, 4 and 6 that showed a limiting available Ni content of 768 μg/g. Thus just over seven croppings at pH 6 in the rhizosphere would reduce the available Ni pool by 30%. A proposed model for phytomining involves harvesting the crop after 12 months and burning the material to produce a sulphur-free bio-ore with about 11% Ni. Utilising the energy of combustion is also discussed. It is considered that Alyssum bertolonii or other Alyssum species might be used for phytomining throughout the Mediterranean area including Anatolia, as well as in Western Australia and the western United States. The economic limits of phytomining are proposed and at current world prices, the technique would only be feasible for Ni and Co with plants of at least the same biomass as Alyssum. Plants of higher biomass and similar uptake potential as for Ni, could extend the limits to other elements.
Article
Full-text available
Soils developed on serpentine rocks cover a large area in Albania which contains large reserves of iron, nickel, chromium and copper and is characterised by a high density of mines and metal smelters. This work was conducted to study the flora associated with serpentine and former industrial and mining sites in Albania. Eight sites were investigated in the south-eastern, central and northern parts of the country. Soils were sampled in the Ap horizon and plants were collected and identified. Plant material was allowed to dry before being ground. Soil and plant samples were analysed for total Ca, Cd, Co, Cr, Cu, Mg, Ni, Pb and Zn. Results showed that each site exhibited a high concentration of one or more metals. The maximum concentrations of metals in soils dry matter (DM) were 14 mg Cd kg-1, 476 mg Co kg-1, 3865 mg Cr kg-1, 1107 mg Cu kg-1, 3579 mg Ni kg-1, 172 mg Pb kg-1 and 2495 mg Zn kg-1. The Mg/Ca ratio in serpentine soils varied from 1 to 7.8. A collection of 58 plant species, members of 44 genera and 17 families, were collected. Alyssum markgrafii in the north and Alyssum murale in the south-eastern serpentines had a concentration of 1.26 and 0.85% Ni in DM, respectively. In the species Herniaria hirsuta, a serpentine plant, concentrations of 808 mg Ni kg-1 and 275 mg Cr kg-1 in DM were recorded. Other taxa (Filago, Inula, Picris, Galamintha, Marrubium, Teucrium, Lotus, Ononis and Xeranthemum) from serpentines had a high, but not exceptional Ni content. Some species collected on serpentines and industrial sites presented rather high concentrations of lead or copper in their above-ground parts, probably related to contamination by soil dust.
Article
Full-text available
Nickel (Ni) hyperaccumulation is a rare form of physiological specialization shared by a small number of angiosperms growing on ultramafic soils. The evolutionary patterns of this feature among European members of tribe Alysseae (Brassicaceae) are investigated using a phylogenetic approach to assess relationships among Ni hyperaccumulators at the genus, species and below-species level. Internal transcribed spacer (ITS) sequences were generated for multiple accessions of Alysseae. Phylogenetic trees were obtained for the genera of the tribe and Alyssum sect. Odontarrhena. All accessions and additional herbarium material were tested for Ni hyperaccumulation with the dimethylglyoxime colorimetric method. Molecular data strongly support the poorly known hyperaccumulator endemic Leptoplax (Peltaria) emarginata as sister to hyperaccumulator species of Bornmuellera within Alysseae. This is contrary to current assumptions of affinity between L. emarginata and the non-hyperaccumulator Peltaria in Thlaspideae. The lineage Bornmuellera-Leptoplax is, in turn, sister to the two non-hyperaccumulator Mediterranean endemics Ptilotrichum rupestre and P. cyclocarpum. Low ITS sequence variation was found within the monophyletic Alyssum sect. Odontarrhena and especially in A. murale sensu lato. Nickel hyperaccumulation was not monophyletic in any of three main clades retrieved, each consisting of hyperaccumulators and non-hyperaccumulators of different geographical origin. Nickel hyperaccumulation in Alysseae has a double origin, but it did not evolve in Thlaspideae. In Bornmuellera-Leptoplax it represents an early synapomorphy inherited from an ancestor shared with the calcicolous, sister clade of Mediterranean Ptilotrichum. In Alyssum sect. Odontarrhena it has multiple origins even within the three European clades recognized. Lack of geographical cohesion suggests that accumulation ability has been lost or gained over the different serpentine areas of south Europe through independent events of microevolutionary adaptation and selection. Genetic continuity and strong phenotypic plasticity in the A. murale complex call for a reduction of the number of Ni hyperaccumulator taxa formally recognized.
Article
Full-text available
Plants that hyperaccumulate Ni exhibit an exceptional degree of Ni tolerance and the ability to translocate Ni in large amounts from root to shoot. In hyperaccumulator plants in the genus Alyssum, free His is an important Ni binding ligand that increases in the xylem proportionately to root Ni uptake. To determine the molecular basis of the His response and its contribution to Ni tolerance, transcripts representing seven of the eight enzymes involved in His biosynthesis were investigated in the hyperaccumulator species Alyssum lesbiacum by RNA gel blot analysis. None of the transcripts changed in abundance in either root or shoot tissue when plants were exposed to Ni, but transcript levels were constitutively higher in A. lesbiacum than in the congeneric nonaccumulator A. montanum, especially for the first enzyme in the biosynthetic pathway, ATP-phosphoribosyltransferase (ATP-PRT). Comparison with the weak hyperaccumulator A. serpyllifolium revealed a close correlation between Ni tolerance, root His concentration, and ATP-PRT transcript abundance. Overexpression of an A. lesbiacum ATP-PRT cDNA in transgenic Arabidopsis thaliana increased the pool of free His up to 15-fold in shoot tissue, without affecting the concentration of any other amino acid. His-overproducing lines also displayed elevated tolerance to Ni but did not exhibit increased Ni concentrations in either xylem sap or shoot tissue, suggesting that additional factors are necessary to recapitulate the complete hyperaccumulator phenotype. These results suggest that ATP-PRT expression plays a major role in regulating the pool of free His and contributes to the exceptional Ni tolerance of hyperaccumulator Alyssum species.
Article
Full-text available
Two strategies of phytoextraction have been shown to have promise for practical soil remediation: domestication of natural hyperaccumulators and bioengineering plants with the genes that allow natural hyperaccumulators to achieve useful phytoextraction. Because different elements have different value, some can be phytomined for profit and others can be phytoremediated at lower cost than soil removal and replacement. Ni phytoextraction from contaminated or mineralized soils offers economic return greater than producing most crops, especially when considering the low fertility or phytotoxicity of Ni rich soils. Only soils that require remediation based on risk assessment will comprise the market for phytoremediation. Improved risk assessment has indicated that most Zn + Cd contaminated soils will not require Cd phytoextraction because the Zn limits practical risk from soil Cd. But rice and tobacco, and foods grown on soils with Cd contamination without corresponding 100-fold greater Zn contamination, allow Cd to readily enter food plants and diets. Clear evidence of human renal tubular dysfunction from soil Cd has only been obtained for subsistence rice farm families in Asia. Because of historic metal mining and smelting, Zn + Cd contaminated rice soils have been found in Japan, China, Korea, Vietnam and Thailand. Phytoextraction using southern France populations of Thlaspi caerulescens appears to be the only practical method to alleviate Cd risk without soil removal and replacement. The southern France plants accumulate 10-20-fold higher Cd in shoots than most T. caerulescens populations such as those from Belgium and the UK. Addition of fertilizers to maximize yield does not reduce Cd concentration in shoots; and soil management promotes annual Cd removal. The value of Cd in the plants is low, so the remediation service must pay the costs of Cd phytoextraction plus profits to the parties who conduct phytoextraction. Some other plants have been studied for Cd phytoextraction, but annual removals are much lower than the best T. caerulescens. Improved cultivars with higher yields and retaining this remarkable Cd phytoextraction potential are being bred using normal plant breeding techniques.
Article
For years, metallophytes of both natural and human-influenced metalliferous soils have focussed considerable attention due to their unique appearance and ability to colonize often extremely harsh habitats. A majority of metal-contaminated areas comprise serpentine (ultramafic, rich in Ni, Cr and Co) and calamine (rich in Zn, Pb and Cd) soils hosting characteristic serpentine and calamine flora, which is the focus of this review. Through microevolution, the plants inhabiting metalliferous habitats have developed a range of intriguing adaptive traits, demonstrated as characteristic morphological, behavioural and physiological alterations that enable them to avoid and/or tolerate metal toxicity. The mechanisms responsible for protection of the plant cell from metals entering the protoplast as well as for detoxification of toxic metal ions inside the cell by chelation, vacuolar sequestration and exclusion from the protoplast are reviewed. These mechanisms have resulted in highly specialized plants able to hyperaccumulate or avoid metals in the shoots. Potential applications of both kinds of metallophytes in rehabilitation and phytoremediation of metal-polluted sites are briefly discussed. Moreover, other beneficial applications of metal-rich plant biomass are mentioned, e. g., as a bio-ore for precious metal recovery (phytomining, agromining), a by-product for eco-catalyst production or a natural source of micronutrients that are essential for human diet and health (biofortification). The need of active protection of metalliferous sites and conservation of metallophyte biodiversity is pointed out.
Article
Introduction of non-native trees is one of the major threats to ecosystem integrity and biodiversity. Stands of maritime pine (Pinus pinaster Ait.) introduced decades ago represent a threat to the specialized plant communities of serpentine outcrops in Italy. This study investigates the effects of such invasions at the community and species level, based on vegetation sampling in three selected sites with comparable environmental conditions. Pine cover caused a decrease of ?-diversity by lowering the species evenness of the community, though species richness was not negatively affected. Compositional changes between the two habitats were significant but not clearly associated with a decrease in taxonomic distinctness in the pine stands. As many as nine indicator species were found in the open vegetation, along with the obligate endemics Odontarrhena bertolonii and Armeria denticulata. Both of them declined in the pine stands. Here, an increase in the phytoavailable nickel fraction was associated with a decrease in total nickel concentration in the soil, via mobilization of the metal caused by lowering of pH induced by the conifer litter. The nickel-hyperaccumulator O. bertolonii was able to maintain high metal concentrations in the shoots despite a decrease in root concentration, resulting in a higher shoot/root ratio in the pine stands (~20). Conversely, shoot/root ratio in the non-accumulator Plantago holosteum was <1 and not affected by the conifer, as well as its abundance in this anthropogenic habitat. Contrasting responses of the two species were likely due to their different sensitivity to modified light and soil conditions, whereas stability of shoot nickel-concentration in O. bertolonii did not support increased predation by natural enemies as one of the causes for its decline under the conifer. Progressive thinning of these stands is advocated to limit soil nickel mobilization and to restore a unique ecosystem with its endemic metallophytes.
Chapter
For years, metallophytes of both natural and human-influenced metalliferous soils have focussed considerable attention due to their unique appearance and ability to colonize often extremely harsh habitats. A majority of metal-contaminated areas comprise serpentine (ultramafic, rich in Ni, Cr and Co) and calamine (rich in Zn, Pb and Cd) soils hosting characteristic serpentine and calamine flora, which is the focus of this review. Through microevolution, the plants inhabiting metalliferous habitats have developed a range of intriguing adaptive traits, demonstrated as characteristic morphological, behavioural and physiological alterations that enable them to avoid and/or tolerate metal toxicity. The mechanisms responsible for protection of the plant cell from metals entering the protoplast as well as for detoxification of toxic metal ions inside the cell by chelation, vacuolar sequestration and exclusion from the protoplast are reviewed. These mechanisms have resulted in highly specialized plants able to hyperaccumulate or avoid metals in the shoots. Potential applications of both kinds of metallophytes in rehabilitation and phytoremediation of metal-polluted sites are briefly discussed. Moreover, other beneficial applications of metal-rich plant biomass are mentioned, e.g., as a bio-ore for precious metal recovery (phytomining, agromining), a by-product for eco-catalyst production or a natural source of micronutrients that are essential for human diet and health (biofortification). The need of active protection of metalliferous sites and conservation of metallophyte biodiversity is pointed out.
Chapter
In the serpentinized habitats of the Balkan Penninsula a specific type of soil is developed which appreciably affects flora and vegetation. A certain number of plant species (serpentinophytes) thrives exclusively in these habitats and animal species are scarce. So far a considerable number of serpentinophytes has been described, but we are of the opinion that the relevant descriptions were rather arbitrary. The status of a certain number of species must be checked because true serpentinophytes may be considered only those plants which thrive on shallow soil or even on the barren rocks so that their root system is in a direct contact with the maternal rock. Vegetation of serpentinized area is very degraded, but on the basis of abundant data it may be concluded that not long ago these terrains were forested. Even today some serpentinized terrains are covered with natural pine, oak and other trees. The pine stumps dug out in village dirt roads prove that these barren areas used to be covered with forests. By applying the method of Braun-Blanquet for the study of serpentinized terrains of the Balkan Peninsula a certain number of communities was described. Some of them are presented in this work. We hope that future investigations with a more detailed approach including ecological and physiological aspects will allow the revision of these communities. In some serpentinized areas soil is denuded to such an extent that natural afforestation is impossible. It must be carried out by seeding or planting.
Article
Ultramafic areas exist in large blocks or as small outcrops separated from other geological substrates in Serbia and host a certain number of facultative serpentinophytes. Among them is Alyssum murale Waldst & Kit. s.l., widespread species distributed in SE Europe and SW Asia and well known example of Ni hyperac-cumulators. The aims of the present study were to investigate the level of concentration of Ni (and some elements such as Fe, Mn, Zn, Cu, Ni, Cr, Pb, Co, and Cd) at several serpentine soils in Serbia and to determine the level of accumulation of these elements in roots, shoots, and leaves, with a focus on Ni. The maximum available concentrations of metals in soil dry matter (DM) were 950 mg·kg-1 Fe, 3,110 mg·kg-1 Ca, 4,600 mg·kg-1 Mg, 443 mg·kg-1 Ni, 803 mg·kg-1 Mn, 26 mg·kg-1 Zn, 4 mg·kg-1 Cu, 43 mg·kg-1 Cr, 82 mg·kg-1 Co, 1 mg·kg-1 Cd, and 17 mg·kg-1 Pb. The Ca/Mg ratio in serpentine soils varied from 0.08 to 6.22. In A. murale plants, the maximum concentrations of Ni were up to 2,926 mg·kg-1 in roots, 6,793 mg·kg-1 in shoots, and 13,160 mg·kg-1 in leaves. Ca/Mg ratio in plant tissues were up to 2.25 (roots), 9.25 (shoots), and 15.23 (leaves). Cu content in the roots and shoots was high (up to 1,044 mg·kg-1 Cu and 849 mg·kg-1 Cu). This survey suggests that some A. murale populations from serpentine soils of Serbia emerge as strong Ni hyperaccumulators and can be used for phytoextraction purposes.
Article
L'auteur a effectué des dénombrements chromosomiques sur une quarantaine d'espèces, appartenant à la famille des Campanulacées, récoltées en Grèce. Plusieurs de ces nombres sont nouveaux.
Article
It has been shown previously that 45 species of Alyssum (Cruciferae), found on serpentine soils, can accumulate nickel to levels above 1000 μg/g (on a dry mass basis). An investigation of most species of the Old World genera of Tribus Alysseae has now demonstrated that this remarkable nickel accumulation is exhibited by five additional serpentine taxa from Turkey and the Balkans: Alyssum peltarioides subsp. virgatiforme, Bornmuellera glabrescens, B. baldaccii, B. tymphaea, and the hybrid B. × petri. All of these taxa had maximum nickel concentrations in the range 1.0-3.1%. Additional data are presented for Alyssum species, including some for taxa not previously reported. Although adaptation by plant species to unfavourable edaphic factors may take place in a relatively short time, it is noteworthy that all species so far recognised as nickel accumulators are from regions that were beyond the maximum advance of the Pleistocene ice-caps. These plants may therefore represent a type of behaviour which started to evolve prior to the most recent glacial episodes. Possible reasons for the endemism of many of the nickel accumulators are outlined.
Article
The diversity of Alyssum section Odontarrhena in the central–western Mediterranean region was investigated to elucidate relationships and biogeography of Ni-hyperaccumulators in the group. Karyological, morphometric and molecular phylogenetic analyses were performed on accessions of Ni-hyperaccumulators from serpentine outcrops and non-hyperaccumulators from calcareous–dolomitic soils in the region. Alpine and Apennine populations of A. argenteum, Sardinian A. tavolarae and some Tuscan A. bertolonii had a tetraploid chromosome complement and larger silicles, seeds and seed wings than diploid accessions. DNA sequences from the plastid rpoC1 locus corroborated the monophyly of section Odontarrhena but species relationships were poorly resolved. Bayesian analysis of combined ITS-rpoC1 sequences retrieved three main lineages including hyperaccumulators and non-hyperaccumulators of contrasting geographical origin. One lineage was mainly continental and included alpine and northern Apennine populations of A. argenteum, the Balkan complex of A. murale and the Iberian group of A. serpyllifolium, sister to Corsican A. robertianum as suggested by their similar diploid karyotype. In this clade no divergence was found between typical A. serpyllifolium and related Ni-hyperaccumulator races from the Iberian peninsula, supporting their conspecific status. A second lineage was prevalently Mediterranean and included the sister species A. bertolonii and A. tavolarae, and other endemics from Sicily, the southern Balkans and Turkey from dolomite and serpentine habitats. The present data suggest new model systems consisting of hyperaccumulators and non-hyperaccumulators of proven phylogenetic affinity for further research on the molecular mechanisms of Ni-hyperaccumulation and serpentine tolerance at the diploid and tetraploid level.
Article
The objective of this article is to use the geology and tectonics of a critical part of the Tethyan orogen, represented by Greece and Albania, to shed light on the tectonic development of Tethys on a regional to global scale. A review of existing Tethyan reconstructions reveals little consensus concerning key aspects, such as the timing and direction of subduction, arc magmatism, ophiolite genesis, and continental collision. The regional to local-scale geology of individual regions, therefore, has to be considered in detail to test existing models and to develop a viable tectonic reconstruction.For Carboniferous time, much evidence suggests that the Korabi–Pelagonian crustal unit as exposed in Albania and Greece formed above a northward-dipping subduction zone along the Eurasian continental margin, with Palaeotethys to the south. However, there is also evidence of southward subduction beneath Gondwana, especially from southern Greece and central-southern Turkey. Palaeotethys is inferred to have closed in Europe as far to the east as the longitude of Libya, although remaining open beyond this region. Uncertainty still exists regarding the Pangaea A-type reconstruction that would restore all the present units in the area within the Eastern Mediterranean region versus the Pangaea B-type reconstruction that would require right-lateral displacement of exotic terranes by up to 3500 km eastwards. In either reconstruction, fragments of the Variscan collisional orogen are likely to have been displaced variable distances eastwards in the Balkan region prior to Late Permian–Early Triassic time. From the ∼Late Permian, the Greece–Albania crustal units were located in their present relative position within Tethys as a whole.From the mid-Permian onwards, the northern margin of Gondwana was affected by crustal extension. A Mesozoic ocean (i.e. the Pindos–Mirdita Ocean) then rifted during Early–Middle Triassic time, culminating in final continental break-up and sea-floor spreading during the Late Triassic (Carnian–Norian). Subduction-influenced volcanics of mainly Early–Middle Triassic age probably reflect the extraction of magma from sub-continental lithosphere that was enriched in subduction-related fluids and volatiles during an earlier Variscan(?) subduction event. The existence of Late Triassic mid-ocean ridge-type igneous rocks, known locally in Albania and Greece, points to rifting of a Red Sea-type oceanic basin rather than a back-arc basin related to contemporaneous subduction. After initial, inferred slow spreading at a Late Triassic, rifted ocean ridge and spreading during the Early Jurassic, the ocean basin underwent regional convergence. Subduction was initiated at, or near, a spreading axis perhaps adjacent to an oceanic fracture zone. The Jurassic supra-subduction zone-type ophiolites of both Greece and Albania largely relate to melting of rising asthenosphere in the presence of aqueous volatiles derived from subducting oceanic lithosphere. High-magnesian boninite-type magmas that are present both in the Albanian and Greece ophiolites and in some underlying melanges reflect remelting of previously depleted oceanic upper mantle. Localized MOR-type ophiolites of Late–Middle Jurassic age, mainly exposed in northeast Albania, were created at a rifted spreading axis. The amphibolite-facies metamorphic sole of the ophiolites was mainly derived from the oceanic crust (including within-plate-type seamounts), whereas the underlying lower-grade, greenschist-facies sole was mainly sourced from the rifted continental margin. The melange, dismembered thrust sheets, and polymict debris flows (olistostromes) beneath the ophiolites formed by accretion and gravity reworking of continental margin units. The in situ radiolarian chert cover of the ophiolites in northern Albania is overlain by polymict debris flows (olistostromes). Pelagic carbonate deposition followed during Tithonian–Berriasian time, and then a regional carbonate platform was restored during the Cretaceous. Exhumation of deeply buried parts of the overridden continental margin probably took place during the Early Cretaceous. Structural evidence, mainly from northern Greece (Vourinos, Pindos, and Othris areas), indicates that the ophiolites, the metamorphic sole, the accretionary melange, and the underlying continental margin units were all deformed by top-to-the-northeast thrusting during late Middle–early Late Jurassic time. However, such kinematic evidence is not obviously replicated in Albania, characterized by reports of ∼southwest-directed (or variable) emplacement. The remaining Pindos–Mirdita oceanic crust subducted ∼northeastwards during Late Cretaceous–Eocene time, whereas oceanic crust continued to form in the south Aegean region at least locally during Late Cretaceous time.During early Cenozoic time, the Pindos–Mirdita Ocean closed progressively southwards, triggering mainly southward progradation of turbidites derived from the overriding Korabi–Pelagonian microcontinent. Smaller volumes of sediment were also derived from the Apulia (Adria) continent. The Mesohellenic Trough of Greece and its counterpart in Albania evolved from an Eocene fore-arc-type basin above subducting oceanic lithosphere to a thrust-top basin as continental crust continued to underthrust during the Oligocene after final closure of the Pindos–Mirdita Ocean. Miocene and Plio-Quaternary successor flexural fore-deeps developed in response to continuing regional plate convergence. The preferred tectonic alternatives are assembled into a new overall tectonic model, which in turn needs to be tested and developed in the light of future studies.
Article
Plants that have evolved to survive on metal-rich soils—metallophytes—have key values that must drive research of their unique properties and ultimately their conservation. The ability of metallophytes to tolerate extreme metal concentrations commends them for revegetation of mines and metal-contaminated sites. Metallophytes can also be exploited in environmental technologies, for example, phytostabilization, phytoremediation, and phytomining. Actions towards conserving metallophyte species are imperative, as metallophytes are increasingly under threat of extinction from mining activity. Although many hundreds of papers describe both the biology and applications of metallophytes, few have investigated the urgent need to conserve these unique species. This paper identifies the current state of metallophyte research, and advocates future research needs for the conservation of metallophyte biodiversity and the sustainable uses of metallophyte species in restoration, rehabilitation, contaminated site remediation, and other nascent phytotechnologies. Six fundamental questions are addressed: (1) Is enough known about the global status of metallophytes to ensure their conservation? (2) Are metallophytes threatened by the activities of the minerals industry, and can their potential for the restoration or rehabilitation of mined and disturbed land be realized? (3) What problems exist in gaining prior informed consent to access metallophyte genetic resources and how can the benefits arising from their uses be equitably shared? (4) What potential do metallophytes offer as a resource base for phytotechnologies? (5) Can genetic modification be used to “design” metallophytes to use in the remediation of contaminated land? (6) Does the prospect of using metallophytes in site remediation and restoration raise ethical issues?
Article
Summary • Molecular phylogeny based on ribosomal internal transcribed spacer (ITS) sequences was studied to investigate the phyletic relationships among some nickel (Ni)-hyperaccumulating and nonhyperaccumulating species of the genus Alyssum in relation to their geographic distribution and Ni-hyperaccumulating phenotype. • Thirty-seven samples belonging to 32 taxa were analysed by sequencing the polymerase chain reaction-amplified ITS region and performing neighbor joining, maximum parsimony and maximum likelihood phylogenetic analyses. • The ITS region in the sampled species varied from 221 to 307 bp of ITS1 and from 194 to 251 bp of ITS2. A total of 765 characters was used to infer the phylogeny and the average nucleotide variation detected was 15.15%. • Nickel-hyperaccumulation could have been lost or acquired independently more than once during the speciation of the genus. The geographical location of species could not be related to phylogenetic affinities.
Article
Serpentine (ophiolithic) substrate covers large areas in the Balkans, more so than in any other part of Europe. These areas extend from north to south mainly in the mountainous central regions and represent specialized habitats for basiphilous-calcifugal plants. Biodiversity in the area is high, with a great number of interesting local and regional endemics. The high number of endemics indicates the importance of serpentine habitats as centres for floristic differentiation and speciation. The number of Balkan endemics growing on serpentine is c. 335 taxa (species and subspecies) of which 123 are obligate. Their distribution is presented in 50 50 km UTM squares as adopted in the Atlas Florae Europaeae project coordinated at Helsinki. The richest (in number of taxa) squares are situated in NW Greece (Epirus), the island of Evvia, N Albania together with SW Serbia, and N Greece (Vourinos). They indicate important centres of plant diversity in the Balkans, areas to be noted for conservation strategy. Features responsible for the distribution and abundance of these obligate serpentine endemics include: 1) edaphic isolation in relation to type of bedrock (lime, dolomite, marble, schist, etc.), 2) mountain island isolation (Smolikas, Vourinos, Ostrovica, etc.), 3) island isolation (Evvia) and 4) continuous long-term isolation without interruption or disturbance of speciation.
Article
Summary 759 Acknowledgements 772 References 772 Metal hyperaccumulator plants accumulate and detoxify extraordinarily high concentrations of metal ions in their shoots. Metal hyperaccumulation is a fascinating phenomenon, which has interested scientists for over a century. Hyperaccumulators constitute an exceptional biological material for understanding mechanisms regulating plant metal homeostasis as well as plant adaptation to extreme metallic environments. Our understanding of metal hyperaccumulation physiology has recently increased as a result of the development of molecular tools. This review presents key aspects of our current understanding of plant metal – in particular cadmium (Cd), nickel (Ni) and zinc (Zn) – hyperaccumulation.
  • O Chalcidica
O. chalcidica (Janka 1872: 175) Španiel, Al-Shehbaz, D.A.German & Marhold in Španiel et al. (2015: 2484).
for checking literature and herbarium collections in B; Cristina Salvatici and Laura Vivona (Florence) for technical assistance, Arne Strid (Copenhagen), and Lefter Kashta (Tirana) for discussion. Anonymous reviewers provided useful comments on the original manuscript
  • H Hartmut
  • Hilger
Hartmut H. Hilger (Berlin), for checking literature and herbarium collections in B; Cristina Salvatici and Laura Vivona (Florence) for technical assistance, Arne Strid (Copenhagen), and Lefter Kashta (Tirana) for discussion. Anonymous reviewers provided useful comments on the original manuscript. This research was conducted in the framework of Agronickel, a FACCE SURPLUS project supported by ERA-NET Cofund. LITErATUrE cITED
Accumulation of Nickel by terrestrial plants
  • R R Brooks
Brooks, R.R. (1980) Accumulation of Nickel by terrestrial plants. In: Nriagu, J.O. (Ed.) Nickel in the Environment. Wiley & Sons, New York, pp. 407-456.
Prodromus florae Peninsulae Balcanicae 1. Pteridophyta, Gymnospermae, Dicotyledoneae (Apetalae et Choripetalae)
  • A Hayek Von
Hayek von, A. (1927) Prodromus florae Peninsulae Balcanicae 1. Pteridophyta, Gymnospermae, Dicotyledoneae (Apetalae et Choripetalae).
Atlas Florae Europeae 11. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo
  • J Jalas
  • J Suominen
Jalas, J & Suominen, J. (1996) Atlas Florae Europeae 11. The Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo, Krämer, Helsinki, 310 pp.
Plantarum novarum turcicarum breviarium
  • V De Janka
Janka, V. de. (1872) Plantarum novarum turcicarum breviarium. Oesterreichische Botanische Zeitschrift 22: 174-182. https://doi.org/10.1007/BF01644772
Synopsis florae germanicae et helveticae. F. Wilmans, Francofurti ad Moenum
  • W D J Koch
Koch, W.D.J. (1836) Synopsis florae germanicae et helveticae. F. Wilmans, Francofurti ad Moenum [Frankfurt am Main], 102 pp. https://doi.org/10.5962/bhl.title.6629
  • K F Ledebour
  • A Bunge
  • C A Meyer
Ledebour, K.F. von, Bunge, A. von & Meyer, C.A. (1831) Flora Altaica 3. G. Reimeri, Berolinum [Berlin], viii + 368 pp. https://doi.org/10.5962/bhl.title.6618
1753) Species plantarum 2. Impensis Laurentii Salvii, Holmia
  • C Linnaeus
Linnaeus, C. (1753) Species plantarum 2. Impensis Laurentii Salvii, Holmia [Copenhagen], 639 [561-1200] + 31 [final, not numbered pages of index, addenda and errata] pp.