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Halophytes——An Emerging Trend inPhytoremediationEleni Manousaki a & Nicolas Kalogerakis aa Department of Environmental Engineering, Technical University ofCrete, Polytechneioupolis, Chania, Greece

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International Journal of Phytoremediation, 13:959–969, 2011Copyright C© Taylor & Francis Group, LLCISSN: 1522-6514 print / 1549-7879 onlineDOI: 10.1080/15226514.2010.532241

HALOPHYTES—AN EMERGING TRENDIN PHYTOREMEDIATION

Eleni Manousaki and Nicolas KalogerakisDepartment of Environmental Engineering, Technical University of Crete,Polytechneioupolis, Chania, Greece

Halophytic plants are of special interest because these plants are naturally present in en-vironments characterized by an excess of toxic ions, mainly sodium and chloride. Severalstudies have revealed that these plants may also tolerate other stresses including heavy met-als based on the findings that tolerance to salt and to heavy metals may, at least partly,rely on common physiological mechanisms. In addition, it has been shown that salt-tolerantplants may also be able to accumulate metals. Therefore, halophytes have been suggestedto be naturally better adapted to cope with environmental stresses, including heavy metalscompared to salt-sensitive crop plants commonly chosen for phytoextraction purposes. Thus,potentially halophytes are ideal candidates for phytoextraction or phytostabilization of heavymetal polluted soils and moreover of heavy metal polluted soils affected by salinity.

Some halophytes use excretion processes in order to remove the excess of salt ions fromtheir sensitive tissues and in some cases these glandular structures are not always specificto Na+ and Cl− and other toxic elements such as cadmium, zinc, lead, or copper are ac-cumulated and excreted by salt glands or trichomes on the surface of the leaves—a novelphytoremediation process called “phytoexcretion.” Finally, the use of halophytes has alsobeen proposed for soil desalination through salt accumulation in the plant tissue or disso-lution of soil calcite in the rhizosphere to provide Ca2+ that can be exchanged with Na+ atcation exchange sites.

KEY WORDS: phytoextraction, phytostabilization, phytoexcretion, heavy metals, salttolerance

INTRODUCTION

Over the last century, public concern about environmental pollution has increasedtremendously. Nowadays, polluted soils and waters as a result of global industrializationpose a major environmental and human health problem, which cannot be easily solved,even in the rich industrialized countries. Classical remediation technologies are mostlyfound inadequate to solve the problem and to redevelop sites for housing, agriculture orrecreation. As a complement to these methods, especially in sites with diffuse low pollutionor in large volumes of water having low concentrations of pollutants, help may be foundin phytoremediation, an emerging technology (Schroder et al. 2002). Phytoremediation,is the use of green plants to remove pollutants from the environment or to render them

Address correspondence to Nicolas Kalogerakis, Department of Environmental Engineering, TechnicalUniversity of Crete, Polytechneioupolis, 73100 Chania, Greece. E-mail: nicolas.kalogerakis@enveng.tuc.gr

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harmless and it is being considered as a new, noninvasive, low-cost, highly promisingtechnology for the remediation of polluted sites (Salt et al. 1998; Arthur et al. 2005). Itutilizes a variety of plant biological processes and the physical characteristics of plantsto aid in site remediation. This technique is potentially applicable to a variety of con-taminants, including some of the most significant such as heavy metals, radionuclides,petroleum hydrocarbons, chlorinated solvents, pentachlorophenol (PCP), and polycyclicaromatic hydrocarbons (PAHs) and it encompasses a number of different methods that canlead to contaminant removal through accumulation (phytoextraction and rhizofiltration)or dissipation (phytovolatilization), degradation (rhizodegradation and phytodegradation),or immobilization (phytostabilization) (Schnoor 1997; USEPA 2001; Pletsch 2003; Pilon-Smits 2005; Fletcher 2006).

Nevertheless, phytoremediation requires more effort than simply planting vegetationand, with minimal maintenance, assuming that the contaminant will disappear. It requiresan understanding of the processes that need to occur, the plants selected, and what needsto be done to ensure plant growth (USEPA 2001). Given the great number of candidates,a relatively limited number of plants have been investigated while another limitation lieswithin the knowledge of basic plant remediation mechanisms, thus, extensive research isneeded upon the identification of suitable plant species that can colonize the polluted areaand remove, degrade or immobilize the contaminant of interest.

Salinity as a stressor induces a wide range of detrimental effects at the cell and wholeplant level. Plant responses to salinity are reasonably well-understood and salt stress resultsfrom a number of detrimental processes including a toxic action of Na+ and Cl− ions, theinhibition of mineral nutrition, a modification in the water status of the plant tissues andsecondary stresses such as an oxidative stress produced by the formation of toxic reactiveoxygen species (Bajji et al. 1998; Orcutt and Nilsen 2000). Plants vary in the degree of theirsalt tolerance and in the means by which they regulate salt content in their tissues. Mostplants are salt sensitive (glycophytes) meaning that these species show little tolerance toelevated root-zone salinity and have decreased growth even at low concentrations of salt.On the other hand, the term halophytes refers to salt tolerant plants that grow on saline soilsand have increased growth at low salt concentrations, with decreased growth at much higherconcentrations (Glenn et al. 1999; Orcutt and Nilsen 2000; Barrett-Lennard 2002; Testerand Davenport 2003). There are two main mechanisms by which halophytes are adaptedto saline environments: salt tolerance, which is the capability to preserve normal metabolicactivity even in the presence of high intracellular salt levels (salt accumulators); and saltavoidance, where the plants do not allow the penetration of salt ions into their sensitive cells.This last mechanism is performed by plants either because the roots have low permeabilityto salts (salt exclusion) or through excretion of some of the penetrating ions and retentionof others (salt evasion) (Mozafar and Goodin 1970; Ramadan 1998; Glenn et al. 1999).Mechanisms very similar to those that seem to function in stress protection in the halophyteshave emerged from the analysis of glycophytic species but their function seems to be slowso they are rather ineffective (Bohnert et al. 1995; Orcutt and Nilsen 2000).

Salt tolerance is a complex trait involving several interacting properties and there isan increasing interest in studying the physiological behavior of halophytic species in orderto identify and understand tolerance mechanisms in general. Moreover, several studies haverevealed that salt tolerant plants may also tolerate other stresses including heavy metalsand xenobiotics offering greater potential for phytoremediation research. The unexploredpotential of halophytes is the scope of the recently initiated COST Action FA0901: PuttingHalophytes to Work—From Genes to Ecosystems (2009–2013). In this manuscript current

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knowledge is summarized concerning the biochemical tolerance mechanisms of halophytesand the prospects of their use for phytoremediation purposes.

TOLERANCE MECHANISMS OF HALOPHYTES AGAINST HEAVY METALS

In the course of evolution, halophyte plants of arid regions became adapted to a setof harsh xerothermic effects, such as extreme air and soil dryness, intense salinization,as well as high summer and low winter temperatures (Shevyakova et al. 2003). Theirability to adapt to environments characterized by an excess of toxic ions (mainly sodiumand chloride) is based mostly on their capability to localize toxic ions in metabolicallyinactive organs and cellular compartments, to synthesize compatible osmolytes, and toinduce antioxidant systems (Glenn et al. 1999; Shevyakova et al. 2003). Therefore, it canbe assumed that halophytes and heavy metal-tolerant plant species possess both specificand general functioning mechanisms of tolerance toward a wide range of abiotic factors(Shevyakova et al. 2003). Available experimental data suggest the hypothesis that toleranceto salt and heavy metals may, at least in part, rely on common physiological mechanisms(Przymusinski et al. 2004). For example, studies by Thomas et al. (1998) on the halophyteMesembryanthemum crystallinum suggest that individual environmental stresses such asNaCl and copper overlap to some extent and one explanation may be that several integratedmechanical and chemical signals are responsible for stress-related responses.

Tolerance of halophytes to the ionic and the osmotic components of salt stress islinked to their ability to synthesize osmoprotectants in order to maintain a favorable waterpotential gradient and to protect cellular structures (Lefevre et al. 2009). Special focus isgiven to proline which is shown to have significant beneficial functions under metal stressby three major actions, namely metal binding, antioxidant defense, and signaling (Sharmaand Dietz 2006), and a large body of data suggests that proline accumulates in responseto Cd, Cu, and other heavy metals (Schat et al. 1997; Thomas et al. 1998; Shevyakovaet al. 2003; Lefevre et al. 2009; Nedjimi and Daoud 2009). Additionally, in a recent studyby Lefevre et al. (2009), it is suggested for the first time that the presence of cadmium maytrigger glycinebetaine oversynthesis which is the most efficient osmoprotectant synthesizedby Chenopodiaceae. Similarly, polyamines may be involved in the protection of cellularstructures under drought and salt stress conditions (Bouchereau et al. 1999) but theirspecific role in plants under metal stress is only poorly documented (Weinstein et al. 1986;Sharma and Dietz 2006; Lefevre et al. 2009). Thus, since heavy metal stress induces both asecondary water stress (Poschenrieder et al. 1989; Nedjimi and Daoud 2009) and oxidativedamages to cellular structures (Briat and Lebrum 1999; Shah et al. 2001; Verma and Dubey2003), the ability of halophytes to synthesize those osmoprotectants may be involved intheir ability to cope with heavy metals (Lefevre et al. 2009).

Furthermore, drought resistance mechanisms may indirectly contribute to heavy metaltolerance, since as already mentioned heavy metal stress is responsible for secondary waterstress in plants in a similar way that salt stress is (Poschenrieder et al. 1989). It has beensuggested that the biological and evolutionary significance of metal accumulation in plantsis connected to drought resistance (Raskin et al. 1994; Boyd and Martines 1998; Macnair2003). Moreover, substantial evidence suggests that the translocation of heavy metals fromroots to shoots is driven mainly by water flux due to transpiration and root pressure (Saltet al. 1995; Nedjimi and Daoud 2009). In addition, the resistance of halophytes to saltstress is usually correlated with a more efficient antioxidant system (Zhu et al. 2004) andhence, halophytes may be more capable to cope with heavy metals stress than common

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Table 1 Salt tolerance mechanisms of halophytes which increase tolerance towards heavy metals

Salt tolerance mechanism induced by heavy metals Selected references

Osmoprotectants synthesis contributes to toleranceagainst metal related stresses (water stress,oxidative stress) and signaling

Thomas et al. (1998); Shevyakova et al.(2003); Lefevre et al. (2009)

Synthesis of antioxidants improve tolerance againstoxidative stress produced by the metals

Zhu et al. (2004)

Salt excretion mechanism contributes to metaltolerance with the excretion of metal ions onto leafsurface

Hagemeyer and Waisel (1988); Manousakiet al. (2008)

plants since as already mentioned heavy metal stress induces oxidative stress to cellularstructures (Briat and Lebrum 1999; Shah et al. 2001; Verma and Dubey 2003). For example,the common ice plant (Mesembryanthemum crystallinum) which is a facultative halophyte,responds to cadmium stress by activation of the peroxidase system, which decreases thedamaging effect of reactive oxygen species (Shevyakova et al. 2003).

On the other hand, according to Bohnert et al. 1995, mechanisms very similar tothose that seem to function in stress protection in the halophytes have emerged from theanalysis of glycophytic species, supporting the hypothesis that stress tolerance mechanismsare ubiquitous. Since stress tolerance is a multigenic trait, the biochemical pathways leadingto products or processes that improve tolerance are likely to act additively and most likelysynergistically. Thus, the advantages of halophytes and xerophytes over glycophytes mayresult simply from the more efficient performance of a few basic biochemical tolerancemechanisms (Bohnert et al. 1995) shown in Table 1. Therefore, halophytes have beensuggested to be naturally better adapted to cope with environmental stresses, includingheavy metals compared to salt-sensitive crop plants, such as, sunflower (Helianthus annuus),corn (Zea mays L.), pea (Pisum sativum L.), and mustard (Brassica juncea L.) commonlychosen for phytoextraction purposes (Jordan et al. 2002; Ghnaya et al. 2005, 2007). Inaddition, it has been speculated that salt-tolerant plants may also be able to accumulatemetals (Jordan et al. 2002) and thus offer greater potential for phytoremediation research.

Besides tolerance mechanisms allowing these plants to cope with internal accumu-lated ions such as sequestration of NaCl in vacuoles and production of compatible osmolytesin the cytoplasm, halophytes have a diversity of secondary mechanisms to handle excesssalt. At the leaf level, some halophytes have salt glands, salt bladders, trichomes or succulenttissues to remove the excess of deleterious toxic ions from photosynthetically active tissuesand regulate plant tissue ion concentration (Glenn et al. 1999; Orcutt and Nilsen 2000;Lefevre et al. 2009). Although not all halophytes have salt excretion organs, in those that do50% or more of the salt entering the leaf can be excreted (Glenn et al. 1999). Salt (mineralsand ions) accumulating glands are mostly common in the following families: Poaceae,Tamaricaceae, Chenopodiaceae, and Frankenaciaceae and many species from these fam-ilies are known to have glandular structures; yet, in most cases further investigations areneeded to determine their secretion products.

Research studies have revealed that in some cases these glandular tissues of halo-phytes are not always specific to Na+ and Cl− and other toxic elements such as cadmium,zinc, lead, or copper are accumulated in salt glands or trichomes while the excretion ofmetals from leaf tissues onto the leaf surface seems to be a method used by these plantsfor dealing with metal burden. For example, studies with the facultative halophyte Tamarix

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aphylla L. have shown that the salt glands are not selective toward sodium and chloride andsecrete Cd and Li ions with a variety of other ions while the composition of secreted saltsis directly related to the composition of the root environment (Thomson et al. 1969; Storeyand Thomson 1994; Hagemeyer and Waisel 1988). Also, in Tamarix smyrnensis Bunge,leaves are covered by salt glands which accumulate and excrete Cd and Pb on the surfaceof the leaves suggesting that this salt tolerant plant uses its salt excretion mechanism toexcrete excess metals on its leaf surface as a possible detoxification mechanism (Manousakiet al. 2008; Kadukova et al. 2008). Moreover, in Atriplex halimus L. which is a hardy xero-halophyte species, leaves are covered by trichomes which accumulate high concentrationof Na+ and Cl− and then burst, leaving salt crystals on the leaf surface. Exposure of theseplants to Cd stress showed that more than 30% of up-taken heavy metals were excreted viathe trichomes outside of the leaf (Lefevre et al. 2009). Likewise, metal excretion throughspecialized glands or glandular trichomes has been observed in mangroves and a number ofother estuarine and salt marsh halophytes such as the marsh-daisy [Armeria maritima (Mill.)Willd.] (Neumann et al. 1995); the gray mangrove [Avicennia marina (Forsk.) Vierh.] (Mac-Farlane and Burchett 1999, 2000); the black mangrove [Avicennia germinans L.] (Sobradoand Greaves 2000); and the salt marsh cord grass [Spartina alterniflora] (Kraus et al. 1986;Kraus 1988; Burke et al. 2000; Windham et al. 2001; Weis and Weis 2004). The presenceof heavy metals has been reported in trichomes of non-halophytes such as Cd, Zn, andPb in tobacco [Nicotiana tabacum L.] (Martell 1974; Choi et al. 2001; Sarret et al. 2006)Cd in Brassica juncea (Salt et al. 1995) Mn in sunflower [Helianthus annuus L.] (Blameyet al. 1986) Ni in the Ni-hyperaccumulator Alyssum lesbiacum (Kramer et al. 1997) or Znand Cd in the hyperaccumulating species Arabidopsis halleri (Kupper et al. 2000).

With the ever increasing demand for agricultural products, the diminishing freshwater resources and the rapid spread of salinity, the concept of saline agriculture is gainingmomentum as cultivation of salt-tolerant crops can help address the threats of irreversibleglobal salinization of fresh water and soils (Rozema and Flowers 2008).

PHYTOREMEDIATION OF HEAVY METALS BY HALOPHYTES

Based on the above, halophytes potentially are tolerant not only to salt but also tometals and other stresses such as chilling, freezing, heat, drought, and many of these plantspecies can grow on land of marginal quality which enables their use for phytoremediation ofsoils with low fertility and poor soil structure, resulting in lower operating costs. Followingthis approach, there is a need for research within the field of phytostabilization for theidentification of high biomass and rapid growth halophytic plants that do not translocatethe metals into their aerial parts, providing a sufficient cover of vegetation that stabilizeslow levels of metals in soils thus preventing metals from mobilizing or leaching intogroundwater, and preventing water and wind erosion.

Furthermore, as already discussed, some salt-tolerant plants are able to accumulatemetals offering a great potential for phytoextraction research. Recent studies focused on thephytoextraction or phytostabilization potential of halophytic plants such as Atriplex halimusL. (Lutts et al. 2004; Lefevre et al. 2009; Manousaki and Kalogerakis 2009; Nedjimi andDaoud 2009), Atriplex nummularia (Jordan et al. 2002), Mesembryanthemum crystallinum(Shevyakova et al. 2003; Ghnaya et al. 2005, 2007), Sesuvium portulacastrum (Ghnayaet al. 2005, 2007), Tamarix smyrnensis Bunge (Kadukova et al. 2008; Manousaki et al. 2008;Manousaki et al. 2009), and salt marsh plants (Reboreda and Cacador 2007, 2008; Sousa

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et al. 2008; Castro et al. 2009) confirm the fact that halophytes are expected to receive moreand more attention by phytoremediation researchers in the near future.

Halophytes may have an additional advantage for phytoextraction applications sincethey can be cultivated with saline irrigation water which is a desirable feature since oftenhigh-quality irrigation water is not available for application to crops in arid regions andhence, brackish waters must be used. Saline water irrigation is becoming an increasinglyimportant practice because the quality of irrigation waters is decreasing as water supplies foragriculture become restricted due to urban needs and climate change (Wahla and Kirkham2008; Rozema and Flowers 2008). Moreover, salinity has been shown to be a key factornot only for the increased bioavailability of metals in the soils due to reduced soil metalsorption (Bingham et al. 1983; Li et al. 1994; Smolders and McLaughlin 1996; Smolderset al. 1998; Norvell et al. 2000; Weggler et al. 2004; Wahla and Kirkham 2008) but also inthe translocation of metals from roots to the aerial parts of the plant (Otte 1991; Fitzgeraldet al. 2003; Manousaki et al. 2008). This is an important feature for phytoextractionapplications since plants that accumulate toxic metals in their above ground parts canbe harvested economically, leaving the soil with a greatly reduced level of toxic metalcontamination. Furthermore, the possible use of phytoremediation for the reclamation ofheavy metal polluted sites affected also by salinity with the use of salt-tolerant plantsbecomes very attractive since the saline depressions often constitute sites of accumulationof industrial effluents contaminated by heavy metals (Jordan et al. 2002; Shevyakova et al.2003; Ghnaya et al. 2005, 2007). For example, preliminary studies carried out in variousregions of Tunisia showed that these zones are contaminated by cadmium, lead, and nickel(Ghnaya et al. 2005, 2007). Therefore, salt-tolerant plants can be viewed as promisingcandidates for the immobilization or the removal of heavy metals not only from regularsoils but also from saline soils as evidenced by recent studies that suggest their use indecontaminating saline soils polluted with metals (Manousaki et al. 2009; Manousaki andKalogerakis 2009; Nedjimi and Daoud 2009).

Recent findings indicate that some salt-tolerant plant species have the ability to excretetoxic metals through specialized salt glands from the leaf tissue onto the leaf surface as amethod of metal detoxification. The term “phytoexcretion” has been recently introducedin the literature to indicate a novel phytoremediation process for sites contaminated withmetals (Kadukova et al. 2008; Manousaki et al. 2008). In Figure 1 the excreted salt dropletscontaining Cd and Pb and crystallized on the leaves of Tamarix smyrnensis due to veryhigh ambient temperatures (>40◦C) are shown. Phytoexcretion brings new potential andopportunities for technological developments as the metals can be collected after theirexcretion before they enter into the soil again. In addition, it was inferred that this methodcould be combined with phytoextraction since plants which have the ability to accumulateand excrete metals may enjoy a unique advantage for phytoremediation applications asthe overall heavy metal removal from the soil is enhanced due to the combined effect ofexcretion and accumulation and this way the frequency of plant pruning is lowered leadingto lower costs and faster remediation times. The idea of using plants as biological pumpsfor heavy metals appears very attractive for the removal of toxic metals from contaminatedsoils and obviously this area deserves further investigation.

PHYTOREMEDIATION OF SALINE SOILS BY HALOPHYTES

Salinization is one of the most serious problems confronting sustainable agriculture inirrigated production systems in arid and semi-arid regions worldwide. The United Nations

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Figure 1 Salt droplets containing Cd and Pb secreted by salt glands were crystallized on the leaves of Tamarixsmyrnensis due to high ambient temperatures (>40◦C). The salt glands of Tamarix sp. secrete with minimalselectivity a variety of different ions and that the composition of the secreted salts is related to the compositionin the rhizosphere. This is the novel “phytosecretion” mechanism of halophytes for phytoremediation purposes(Kadukova et al. 2008). (Color figure available online).

Environment Programme estimates that approximately 20% of agricultural land and 50%of cropland in the world is salt stressed (Ravindran et al. 2007). Salt-impacted soils containexcessively high levels of sodium that as already discussed, can adversely affect plant growthvia osmotic and ionic effects, as well as disruption of nutrient uptake. The ameliorationprocedure for such soils needs proper amendments as a source of calcium (Ca2+) to replacesodium (Na+) from the cation exchange sites. The displaced Na+ is leached from the rootzone through excess irrigation, a process that requires adequate flow of water through thesoil (Qadir et al. 2003). As a potential substitute of cost-intensive chemical amelioration,phytoremediation of saline-sodic soils has been found to be an efficient and low-coststrategy (Qadir and Oster 2002; Qadir et al. 2003). Phytoremediation of these soils involvescultivation of certain salt tolerant plant species with the ability to increase the dissolutionof soil calcite (CaCO3) in the rhizosphere to provide Ca2+ that can be exchanged with Na+

at cation exchange sites. Displaced Na+ can subsequently be leached out of the soil withirrigation water. This process ultimately results in a marked decrease in soil salinity levelsand several plant species of agricultural significance appear suitable to be an effectivephytoremediation tool (Qadir and Oster 2002; Qadir et al., 2003, 2004; Gerhardt et al.2006).

Furthermore, salt-accumulating halophytes have the ability to receive and accumulatequite high concentrations of salts and Na+ in their shoots making them ideal candidatesfor phytoremediation of saline soils, as removal of the aerial parts would remove salt fromthe soil with no need of the leaching step with irrigation water. For instance, Atriplexnummularia has been shown to achieve a biomass yield of 20–30 t ha−1 year−1 andaccumulate up to 40% NaCl in its dry matter (Ghnaya et al. 2005). These and similar otherattributes have led researchers to suggest that halophytes could be grown on salt-affectedsoils to remove significant amounts of salt and Na+ through their aerial parts to the pointthat the soil can be returned to agricultural productivity (Chaudhri et al. 1964; Gritsenkoand Gritsenko 1999; Owens 2001; Keiffer and Ungar 2002; Gerhardt et al. 2006; Ravindran

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et al. 2007). This alternative phytoremediation method for soil desalination can be facilitatedby tailoring plant selection to site conditions, using inputs of fertilizer and water to enhancethe growth of the halophytes and by harvesting the plants on a regular basis (Keiffer andUngar 2002).

CONCLUDING REMARKS

Within the field of phytoremediation, halophytes have been suggested to be betteradapted to cope with heavy metals compared to salt-sensitive plants commonly chosen forphytoextraction or phytostabilization studies; thus halophytes are promising candidates forthe removal or stabilization of heavy metals not only from heavy metal polluted soils butalso from heavy metal contaminated sites affected by salinity since saline depressions areoften encountered in industrial contaminated sites. “Phytoexcretion” has been recently iden-tified as an additional phytoremediation process which is coupled to phytoextraction andprovides opportunities for technological innovation. Moreover, the use of salt-accumulatinghalophytes can be viewed as an alternative phytoremediation method of soil desalination.In a nutshell, halophytes present an emerging trend in phytoremediation research and areexpected to receive considerable attention in the near future.

ACKNOWLEDGMENTS

The project was funded by the European Economic Area Financial Mechanism GrantEL-0075.

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