Dendroremediation of Heavy Metal Polluted Soils

REVIEWS ON ENVIRONMENTAL HEALTH VOLUME 23, NO. 3, 2008

Dendroremediation of Heavy Metal Polluted Soils

J.A. González-Oreja,1† M.A. Rozas,2† I. Alkorta3 and C. Garbisu1

1NEIKER-Tecnalia, Basque Institute of Agricultural Research and Development, Derio;

2Dept. of

Biology and Plant Production, University of Extremadura, Badajoz; 3Biophysics Unit, University of

the Basque Country, P. O. Box 644, Bilbao, Spain

Abstract: Heavy metals are among the most common and harmful pollutants reaching the soil ecosystem all over the

world. Phytoextraction is an effective, non-intrusive, inexpensive, aesthetically pleasing, socially accepted, highly

promising phytotechnology for the remediation of soils polluted with heavy metals. To overcome the so-called

‘Achilles’ heel’ of phytoextraction, namely, the long time needed for effective remediation, this phytotechnology should

be combined with other profit-making activities such as forestry or bioenergy production. Dendroremediation, or the

use of trees to clean up polluted soil and water, appears of great potential for metal phytoextraction, especially when

using fast-growing tree species, for example, willows (Salix sp. pl.) and poplars (Populus sp. pl.). Most important, the

ecologic and environmental risks of dispersing heavy metals into the ecosystems by dendroremediation strategies

should be minimized by selecting the right tree species, properly managing/disposing the polluted plant material, or a

combination of both options.

Keywords: para-phytoremediation, phytoextraction, phytoremediation, phytostabilization, trees Correspondence: Dr. Carlos Garbisu, NEIKER-Tecnalia, Basque Institute of Agricultural Research and Development, Dept of Agroecosystems and Natural Resources, c/ Berreaga, 1; E-48160 Derio (SPAIN); E-mail: [email protected] † Each author contributed equally to the research.

DISCHARGE OF POLLUTANTS INTO THE

ENVIRONMENT AND SOILS

All living beings are known to modify their environment and, in this respect, we humans are no exception. But in the last decades, driven mainly by population growth and rampant consumerism, the damaging effects of human activities on natural ecosystems are reaching dramatic levels: “no ecosystem on Earth is free of pervasive human

impacts” /1/. Traditionally, massive industrializa-tion, unsustainable agricultural practices, and highly inadequate waste disposal methods have been the anthropogenic activities most adversely affecting soil, water, air and biota; yet, only recently has the magnitude of these impairments been transferred from Lilliputian to Gulliverian scales /2/.

That the alteration of the biogeochemical cycles is one of the most negative consequences of human activities on the environment is well recognized /1/. Indeed, a great variety of chemical elements, compounds, and pollutants of all kinds (from nutrients and pesticides to oils and metals) is delivered to the environment on a daily basis /2/; in reality, the reported annual human production and mobilization of many chemical elements of the periodic table equates that of nature /3/.

Certainly, the release of pollutants into the environment has been augmented enormously over the past several decades /4/. Consequently, the increment in the concentration of pollutants in, for instance, many agricultural soils (the source of most of our food), due to unsustainable agricultural practices like the excessive application of artificial

J.A. GONZÁLEZ-OREJA ET AL

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fertilizers and pesticides, is at the moment detrimentally affecting crop production as well as human and ecosystem health. We must remember that a healthy human society is impossible without healthy ecosystems, and that the negative impact of polluting agricultural practices on agrosystems and natural ecosystems must be considered a serious threat to the health of our society /5,6/.

Soils are critical components of ecosystems because soils function not only in the production of food and fiber but also in the maintenance of environmental quality worldwide /7/; indeed, whatever occurs in the soil can affect not only the pedosphere itself but also the hydrosphere, atom-sphere, and biosphere. In any event, defining soil health is a daunting task and its quantification is anything but straightforward /8,9/. Whatever the case may be, soil health or quality (both terms are frequently used interchangeably) has been defined as “the continued capacity of a soil to function as a vital living system, within ecosystem and land-use

boundaries, to sustain biological productivity,

promote the quality of air and water environments,

and maintain plant, animal and human health” /10/. Coleman and coworkers /11/ stated that the health of all groups of living organisms (including soil microorganisms) should be explicitly considered when determining soil health. In this respect, many pollutants released into the soil environment are known to be harmful or toxic to the soil (micro)biota. Finally, as compared to physicochemical properties, biological indicators of soil health are becoming increasingly used because of their sensitivity, rapid response, and capacity to provide information that integrates many environmental factors /8,9, 12-15/.

Heavy metals are among the most common and harmful pollutants affecting soil health all over the world. Heavy metals can be present in soils as natural components or as by-products of different human activities, such as the burning of fossil fuels, the mining and smelting of metalliferous ores, municipal wastes, and others. Several metals are essential for biological systems (they provide

cofactors for metalloproteins and enzymes), yet at high levels, such metals can act in a deleterious manner by altering or blocking essential functions /16/. On the other hand, some non-essential metals are always toxic for life forms and can be tolerated only at minute concentrations. Because of their immutable nature, pollution by heavy metals is of much ecologic and environmental concern /17/. Unfortunately, at present, the massive introduction of these immutable highly toxic pollutants into the recipient soil ecosystems has overwhelmed their self-cleaning capacity. Consequently, widespread metal pollution has caused vast areas of land to become not only unproductive but hazardous for wildlife and humans as well.

The magnitude of this accumulation of heavy metals (and other pollutants) in our soils is calling for immediate action. Unless remediation action is taken, among other aspects, the availability of arable land for cultivation will diminish. Regrettably, most current regulations governing metal toxicity in soils are based on total metal concentrations, ignoring that a major factor governing the toxicity of metals in soil is their bioavailability /18/.

Finally, most important, cleaning up (metal) polluted sites is essential for ensuring the sustainable development of our society, concomitantly reducing the pressure to expand human settlements into the wilderness, forests and marginal lands, thus supporting biodiversity and the preservation of vital ecosystems /19/.

PHYTOREMEDIATION OF HEAVY

METAL-POLLUTED SOILS

Aggressive engineering-based techniques are typically applied to the cleanup of polluted soils, although frequently they are not cost-effective or environmentally justified /20/. Many physical and chemical technologies for the remediation of polluted soils (for example, excavation and ‘final’ disposal to a landfill, capping and containing the polluted areas of a site, and others), besides being

DENDROREMEDIATION OF HEAVY METAL POLLUTED SOILS

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economically very unattractive, do not alleviate environmental hazards at all because the pollution problem is simply relocated in space or time. For example, the remediation of metal-polluted soils by excavation and burial has been stated to have an average cost of $1,000,000 per acre /21/. In reality, the usually enormous costs associated with the removal of metals from soils by means of common physical and chemical methods explains why most companies have tended to ignore the problem /22/. In consequence, non-engineering processes of in situ remediation of polluted soils are clearly worth exploring /23/. Developing ‘soft’ (environmentally friendly), innovative technologies to remediate our deteriorated soils economically while reducing the threats to ecosystems and humans is imperative /17/.

Bioremediation

Because of its potential effectiveness, its comparative low cost and its adaptability to specific scenarios, bioremediation, defined as “a managed treatment process that uses (micro)

organisms to degrade and transform chemicals in

contaminated soil, aquifer material, sludges and

residues” /24/, appears a valid option to ameliorate environmental pollution /4,17,25,26/. Given that it can treat pollution in situ—many of the costs of conventional clean-up physicochemical technol-ogies are linked to physically removing/disposing of polluted soils) /4/—bioremediation can signifi-cantly reduce the economic costs associated with clean-up schemes /27/.

Bioremediation exploits the genetic diversity and metabolic variety of microorganisms like bacteria or fungi for the biotransformation of pollutants into less harmful forms that can then be integrated into natural biogeochemical cycles /28/. Regarding metal pollution, microorganisms can detoxify metals by valence transformation, extra-cellular precipitation, or volatilization /29/. Notwithstanding such microbial abilities, micro-organisms are not effective as a large-scale solution to heavy metal soil pollution because soil

microbiota cannot solve the problem of the removal/extraction of heavy metals from the polluted site /30/. Thus, the use of microorganisms for the in situ bioremediation of heavy metal-polluted soils is largely restricted to metal /31/. Furthermore, effective remediation frequently implies the final removal of the polluted biomass (microbial biomass) from the site and, so far, no cost-effective way exists for retrieving small organisms from the soil /32/. By contrast, plants can literally extract metals from polluted soils, theoretically rendering them clean (metal-free soils) /33/.

Phytoremedation

Phytoremediation, also referred to as botanical remediation or green remediation /34/, has been defined as “the use of green plants to remove environmental contaminants from the environment

or to render them harmless” /19,22,30,33,35-41/. Phytoremediation, a non-intrusive, relatively inexpensive way of remediating polluted soils, is certainly more cost-effective than alternative mechanical or physicochemical methods of removing hazardous compounds from soils /42/. Glass /43/ estimated that the total cost for some phytoremediation schemes would be between 50% and 80% lower than other options. In the same vein, Blaylock and coworkers /44/ estimated that the cost of excavating and landfilling Pb-polluted soils increased to $500/acre, whereas a 50% to 65% saving ($150-250/acre) for phytoextraction was reported. Moreover, phytoremediation is a natural, aesthetically pleasing phytotechnology /45/, acknowledged by human communities and regulatory agencies as a potentially elegant green technology /46/. Finally, phytoremediation is considered a highly promising phytotechnology for the remediation of soils polluted with both organic /39/ and inorganic /33/ compounds, including toxic metals and radionucleids /45/.

Metalliferous soils with abnormally high concentrations of metals vary widely in their


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effects on plant species. Some plants, namely, metallophytes, have evolved the capacity to survive on metal-rich soils /47/ and can function, as solar-driven pumps, to extract and concentrate metals from their environment /36/. In this respect, plants can be considered the “green liver of the Earth” /19/.

Phytoextraction, one of the different strategies included within the term phytoremediation /22/, defined as “the use of plants to remove contaminants from soils into the harvestable parts of

roots and above-ground shoots” /48/, is recognized as a most promising phytotechnology for the remediation of metal polluted soils (but see /49/ for a thoughtful critique and /50/ for a quantitative meta-analysis of recently published results). Desirably, plants for metal phytoextraction should exhibit the following characteristics: • be tolerant to high concentrations of the metals, • accumulate reasonably high quantities of the

metals, • have a rapid growth rate, • produce notable biomass in the field, • have a high shoot-root ratio, and • a profuse root system /30,33/.

By means of phytoextraction, heavy metals can be transported from the soil and concentrated into the aboveground plant tissues, which can then be harvested by conventional methods. The resulting biomass of contaminated plant material can be further reduced in volume and/or weight by composting, anaerobic digestion, ashing, or leaching /19/. Metal-enriched plant biomass can be disposed of as a hazardous material or, if economically viable, used in metal recovery processes /37/.

Some naturally-occurring plants, termed hyper-accumulators, have the capacity to tolerate, to take up, to translocate, and to accumulate in their shoots very high levels of metals over the entire growth cycle /13,15,34/. In recent years, a great deal of research has been conducted on the physiology and biochemistry of metal hyperaccumulation /38,51,52/.

Regrettably, most hyperaccumulators are of small size, have slow rates of development, and we lack the technology for their cultivation at large-scale schemes /36/.

Accordingly, investigation has also been directed toward the metal-accumulating capacity of fast-growing, high biomass crop plant species that can be easily cultivated by common agronomic practices /53,54/. In this respect, to increase soil metal bioavailability and phytoextraction capacity of high biomass plants, chelating agents can be added to the soil /14,53,55/. The application of chelates increases the translocation of heavy metals from soils to plant shoots /36/. This type of chemically/chelate enhanced, assisted, or induced phytoextraction has been proposed as an alternative to the use of hyperaccumulators for the remediation of metal polluted soils /38/. In particular, this approach is applicable in situations in which metal mobility is very low and for those elements for which no hyperaccumulators are known /37/.

Nevertheless, technical, economical and, above all, environmental reservations about the applic-ability of chelate-induced phytoextraction remain /22,40,44/. For instance, ethylenediaminetetra-acetic acid (EDTA), the most commonly used chelating agent in chelate-induced phytoextraction, is poorly degraded in soils where it can persists for long periods /56/. On the other hand, EDTA and many other chelating agents are toxic for plants, /38,56,57/. Unfortunately, chelate-assisted phyto-extraction is likely to enhance the environmental risks of adverse effects due to metal mobilization and leaching during prolonged times. Environ-mentally safe methods must be developed before steps are taken toward further development and commercialization of this phytotecthnology /22, 40/.

Genetic engineering. One way to increase the array of plants available for phytoextraction is to use genetic engineering tools to insert into selected plants those genes that will enable them to tolerate and accumulate heavy metals /41,51,58,59/. Yet,


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until now, only a few cases have been reported for which metal tolerance, uptake, translocation, and accumulation have been successfully altered. At present, the performance of the transgenic plants generated so far is not sufficient for commercial phytoextraction /41/. In any event, we must remember that public concern over the release of genetically modified organisms might force regulators to veto their use /22/.

Phytostabilization. Finally, the use of plants to reduce the bioavailability of pollutants in the environment, phytostabilization, has great potential for the remediation of metal polluted soils /22/. Metal phytostabilization refers to immobilizing metals in soil through root absorption and adsorption, and precipitation within the root zone of plants, preventing contaminant migration via wind and water erosion, leaching, and soil dispersion.

Nevertheless, despite intensive research on metal phytoremediation, only a small number of commercial operations have been carried out /60, 61/. To overcome the so-called ‘Achilles’ heel’ of phytoextraction, namely, the long time needed for effective remediation, some have suggested that this phytotechnology should be combined with other profit-making activities like phytomining (the use of plants to concentrate valuable metals, for example, nickel (Ni) or gold (Au) that can be recovered through metallurgical processes), forestry, or bioenergy production. If these multipurpose environmental cleanup strategies render economic benefits, then the time required for the operation becomes less important /62/. In this respect, much effort is being directed toward the use of trees for soil remediation.

DENDROREMEDIATION

Introduction to dendroremediation

Dendroremediation, or the use of trees to clean up polluted soil and water, appears of great

potential for the phytoextraction and phyto-stabilization of metal polluted soils. In general terms, trees are woody plants with the most stable and massive root systems of all, which penetrate in soils further than most herbaceous species, provide substantial ground-water pumping capabilities, and have a large above-ground biomass that can be harvested at low cost, without (much) disturbing the site. Besides, certain trees are very good competitors for such resources as light, nutrients and water, and tend to dominate the structure of plant communities whenever the ecologic conditions are favorable for plant growth. Interestingly, a number of tree taxa have developed evolutionary mechanisms to cope with highly variable biotic and abiotic stresses and can naturally grow on suboptimal, low-fertility sites with poor-soil structure like, for instance, polluted mines.

Finally, for centuries, man has grown trees for a number of uses, such as energy production, furniture and building material, fiber, and paper, and so on. These and other features make trees a very good candidate for the restoration of degraded landscapes and environments. Not surprisingly, the cultivation of (fast-growing) tree species has been used to remediate heavy metal polluted soils /23,63-66/. Indeed, afforesting polluted sites can be part of a low-cost, in situ reclamation strategy for bringing polluted sites into productive use because trees can remain healthy for many years, even in the presence of extremely high levels of contamination /23/.

In addition to environmental remediation, recognizing concurrent and post-remediation uses for trees employed in phytoremediation is currently a topic of great interest. In this respect, mixed-purpose strategies within the phytoremediation field have been termed “para-phytoremediation” /20/ drawing on the meanings ‘beside’, ‘alongside’, and ‘beyond’ for the prefix ‘para’. Thus, mixed-purpose dendroremediation appears as a cost-effective alternative for large areas of unused lands contaminated by urban or industrial activities /59/. Para-phytoremediation includes, for example, environmental cleanup together with forestry for


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bioenergy production, nutritional enhancement of crops on polluted sites with limited utility, or metal recovery and the recycling of material with commercial value /20/. Interestingly, linking pollutant removal with woody biomass production offers an economic alternative that cycles pollutants into value-added products /64,67/. Among others, primary and secondary products from trees include bioenergy (a cleaner, cheaper and more environmentally acceptable approach to energy production than coal or fuel alone), pulp and paper (which would help take pressure off natural forests), solid wood products (structural lumber, boxes, furniture components, interior trims, etc.), composite wood products, feed products, and so on. Most important, trees have the capacity to reduce the presence of greenhouse gases in the lower atmosphere (namely, carbon sequestration) and to control soil erosion.

Above all, biomass for energy production systems based on tree planting and management can be economically, ecologically and environ-mentally sustainable /67,68/. Wood biomass can produce comparable energy production to coal and, due to its low sulfur content, burns more cleanly and cheaply. Energy production proposals have been implemented for fast-growing, short-rotation trees used to remediate wastewater and sludges from waste water treatment facilities /67,69/. For this purpose, woods with a high specific density and low moisture content should be chosen to enhance yield while reducing additional costs like that of transportation. A high calorific value of the biomass, together with a low ash production, benefits users as well /67/.

Dendroremediation of heavy metal polluted soils

Plant species have a wide norm of reaction to metal toxicity, providing both tolerant and non-tolerant genotypes with the capability for major phenotypic adjustment to metal stress. In addition, a large variability among individual tree species and clones in their ability to take up, translocate,

and accumulate heavy metals in shoots and other above-ground aerial parts has been described /23, 64,66,70/.

For phytoextraction, trees can remove signif-icant amounts of heavy metals from polluted soils by repeated coppicing of the aerial biomass. On the other hand, through phytostabilization, trees can render soils harmless and reduce the risk of further environmental degradation by leaching or airborne spread /30/. Finally, although plants with shallow roots are appropriate for contamination near the surface, trees, due to their deep roots, also show great potential for the in situ remediation of groundwater and deep soil contaminated with toxic elements like, for instance, arsenic /71,72/.

Surprisingly, limited information exists on the response of trees to levels of metals. Watmough and Dickinson /73/ studied the resistance of tissue cultures of sycamore maples to metals (Cu, Cd, and Zn. Wisniewski and Dickinson /74/ evaluated the toxic effects of Cu on the performance of seedlings of English oaks, Quercus robur. Mertens and coworkers /75/ investigated the potential of five different tree species (namely, sycamore maples, black alders, common ashes, white poplars, black locusts) for the dendroremediation of dredged sediments polluted with both organic contaminants and heavy metals. Fuentes et al /76/ carried out a comparative analysis of the phytotoxic effects of Cu, Ni, and Zn on seedlings of four Mediterranean woody species (Juniperus oxycedrus, Pistacia lentiscus, Pinus halepensis, Rhamnus alaternus).

In any event, the evidence is growing that the most efficient phytoextraction of heavy metals through dendroremediation is achieved by means of using different species, hybrids, and clones of willows and osiers (Salix sp. pl.), and of poplars, aspens, and cottonwoods (Populus sp. pl.). These tree species (a) are easy to propagate rapidly (they can be easily reproduced with cuttings and grow rapidly in short-rotation systems); (b) have large and deep root systems (a high proportion of their roots are less than 1 mm in diameter, which


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provides the surface area needed for fungi to form useful mycorrhizae); (c) take up large quantities of water; and (d) achieve high above-ground biomass production /64,70,77-81/.

Certain willow and poplar varieties do not retain elements in their roots but rather transfer them to the above-ground plant tissues, opening prospects for cleaning heavy metal polluted soils through repeatedly harvesting the produced biomass in carefully managed and monitored forestry systems /70,80/. On the other hand, this approach raises environmental concerns of increased heavy metal mobility in natural ecosystems and a risk of food chain contamination (see below). A most important advantage of willow and poplar tree species in remediation schemes, as compared with most known hyperaccumulators, is their much greater harvestable biomass; actually, these species are collectively considered high metal-accumulator trees with great biomass production /77,82/. Nonetheless, wide intraspecific and interspecific differences have been described in studies on the metal remediation efficiency of willow and poplar. In general, many species or clones of Salix have the capacity to bioaccumulate elevated levels of Cd and Zn in above-ground biomass compartments /79,80,82-84/. In turn, Populus trees take up more Pb /82/.

Robinson and colleagues /83/ studied the Cd tolerance and accumulation by clones of both willow (‘Tangoio’, Salix matsudana x S. alba NZ 1040) and poplar trees (‘Kawa’, Populus deltoides x P. yunnanensis NZ 5006; ‘Beaupré’, P. tricocopa x P. deltoides, and ‘Argyle’, P. deltoides x P. nigra NZ 5015) grown in soils under a range of Cd levels. Although plant levels of Cd always exceeded the respective soil levels, bioaccumulation factors showed that Tangoio (willow clone) accumulated significantly more Cd than any poplar variety. Their results indicate that both Salix and Populus have excellent potential for Cd phytoremediation, but willows are more suitable because of higher bioaccumulation factors /80/. After calculating the corresponding metal bioconcentration factors (plant

metal concentration/soil metal concentration; a value > 1 indicates that the plant actively accumulates the metal in its tissues) in two willow clones (S. fragilis ‘Belgisch Rood’ and S. viminalis ‘Aage’), the authors concluded that willow trees are shoot accumulators of Cd and Zn, but root accumulators of other metals (Cu, Cr, Ni and Pb). In 2003, Meers et al /85/ observed that S. dasyclados ‘Loden’ extracted significantly more Zn from dredged, polluted sediments than both S. viminalis ‘Orm’ and S. schwerinii x S. viminalis ‘Tora’. In a related study in 2007, Meers et al. /70/ reported that among five willow clones (S. dasyclados Loden, S. triandra ‘Noir de Villaines’, S. fragilis ‘Belgisch Rood’, S. purpurea x S. daphnoides ‘Bleu’, S. schwerinii ‘Christina’) the shoot accum-ulation of Cu, Cr, Ni, and Pb did not vary and was so low as to be deemed insufficient for phyto-extraction purposes. The authors also found that, out of all the clones under study, Christina, Loden, and Belgisch Rood exhibited the highest Cd and Zn concentrations in stems and leaves, and thus deserve additional attention in future research under field conditions. Taking into account that the accumulation of heavy metals occurs predominantly in actively growing tissues, Meers et al /70/ suggested that, to optimize phytoextraction and export of heavy metals, one should remove foliar material by collecting leaves after they have fallen or by harvesting trees while they are still carrying leaves (see also /81/ for a related suggestion). Combining the estimations of heavy metal concen-trations in soils and uptake by trees, Klang-Westin and Eriksson /77/ concluded that the annual, net removal of Cd from top-soil layers by Salix crops under different environmental conditions varies from 2.6 to 16.5 g Cd ha–1. If these values were sustained all the years that a Salix stand is considered to remain productive, the cropping of willows could ideally be used to counteract the Cd accumulated in the past in agricultural soils /77/. In a related approach, the expected Zn mass to be annually extracted by the best willow accumulator, Christina, was estimated by Meers /70/ to be about


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14-27 kg ha–1, whereas the removal of Cd by other clones was calculated to be 0.25-0.65 kg ha–1, depending on soil type, pollution level, and actual biomass production in field situations.

A limitation of using willows for metal phyto-extraction is that metal removal takes time; thus, cultivation of Salix may not be suitable if fast reduction of heavy metal levels in soil is required /77/. Nonetheless, if dendroremediating willows are grown on mixed-purpose schemes, for instance, as a source for biofuel, the output of Cd via stem harvest can be regarded as a bonus. In this respect, their high biomass yield and high Cd uptake make Salix trees suitable as both phytoextractors of Cd and woody biomass producers in mixed-use dendroremediation plans. After calculating an indicator of wood quality in three willow species (S. discolor, S. petiolaris, and S. viminalis), namely. a combined index that considers the calorific value and the gravity of the wood as positive characteristics, and high water content and high ash as negative properties, S. viminalis was identified by Labrecque and colleagues /67/ as the most promising species in mixed-purpose dendroremediation plans.

Ecologic concerns in dendroremediation

The uptake and translocation of pollutants in trees depends on the concentration of the pollutant in the soil solution, its efficiency in entering the root system, and the rate of transpiration /65/. Ultimately, the efficiency of metal phytoextraction procedures depends on the multiplication of two factors: biomass yield × metal concentration in biomass. Although both factors are certainly important, high concentrations in the above-ground plant parts are most desirable because harvesting roots and other below-ground organs is very difficult /38/.

Because of the large evapotranspiration potential of trees /64/, the possibility exists that heavy metals and other pollutants might be accumulated in large quantities in aerial tree parts. Such

accumulation has been identified as an ecologic risk in dendroremediation measures /86,87/. The same concerns expressed regarding the post-harvest use of crops grown on metal-polluted soils /20/ should be taken into account when considering the fate of heavy metal-accumulating trees through food chains and trophic webs in nature. At certain heavy metal polluted soils and disposal sites, trees used for dendroremediation purposes can absorb and accumulate enough contaminants that stems and leaves are classified as “toxic” /64/. Should herbivore animals consume these or other parts of the trees, such as twigs or seeds, then an exposure pathway could be initiated for toxic elements to enter local food webs /88/. Actually, elevated metal concentrations in living plant tissues pose a risk not only for the immediate trophic level, the primary consumers (herbivores), but also for subsequent, secondary consumers (carnivores, such as insects, birds, and mammals at higher trophic levels) or decomposers, causing dispersal into the ecosystem.

Yet, this aspect is not the only risk derived from the accumulation of metals in the above-ground biomass: polluted plant material can be dispersed to adjacent environments and then metals could accumulate in the upper soil horizons as well, especially those associated with organic matter /61/. In any case, information is generally lacking for the accurate assessment of the risks posed by the metal polluted biomass on the rest of the ecosystem (for example, possible behavioral mechanisms implying the avoidance of polluted plant parts, secondary poisoning through the food chain) /61/.

Most important is that whenever metal phyto-extraction or phytostabilization is chosen as a remediation technique, the risks of pollutant dispersal into the environment should be minimized /75/. In phytostabilization, this goal can be achieved by choosing tree species that do not accumulate heavy metals in their aerial parts, thus reducing access to the toxic metals. Taking into account their low metal concentrations in above-ground tissues, tree species like black alders, Alnus


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glutinosa; common ashes, Fraxinus excelsior; or sycamore maples, Acer pseudoplatanus, might be suitable for phytostabilization purposes /75/. If leaves and leaf fall from trees pose a serious risk, then harvesting them in addition to the wood could be a reasonable management option to reduce the risks of trophic web accumulation /79/. In the case of phytoextraction, the post-harvest disposal of plant material as hazardous waste and, when possible, the recovery and reuse of metals from plants, have been considered /64/.

CONCLUSION

Trees, and particularly fast-growing species such as willows (Salix sp. pl.) and poplars (Populus sp. pl.), have great potential for the remediation of metal-polluted soils. Most important, if metal removal is linked to biomass production in mixed-purpose plans, then economic alternatives turn up into value added products (for example, bioenergy). In any case, ecologic and environmental risks of dispersing heavy metals into ecosystems by dendroremediation strategies should be minimized by selecting the right tree species, properly managing/disposing the polluted plant material, or a combination of both options.

Nevertheless, as dendroremediation requires long time periods and no tree species is known to accumulate simultaneously a considerable variety of the most environmentally toxic metals, one might argue that the feasibility of phytoextraction by planting trees is doubtful (many sites for remediation are simultaneously polluted with a variety of heavy metals). For instance, although visual appearance is certainly enhanced and trees help to phytostabilize metals in soils, the use of willows or poplars for phytoextraction has the disadvantage that the polluted soil will only be cleaned from Cd and Zn.

To better exploit trees for dendroremediation schemes, much further research is necessary.

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Dendroremediation of Heavy Metal Polluted Soils