areviewonheavymetals(as,pb,andhg)uptakeby ...heavy metals are conventionally defined as elements...
TRANSCRIPT
-
Hindawi Publishing CorporationInternational Journal of Chemical EngineeringVolume 2011, Article ID 939161, 31 pagesdoi:10.1155/2011/939161
Review Article
A Review on Heavy Metals (As, Pb, and Hg) Uptake byPlants through Phytoremediation
Bieby Voijant Tangahu,1 Siti Rozaimah Sheikh Abdullah,2 Hassan Basri,1
Mushrifah Idris,3 Nurina Anuar,2 and Muhammad Mukhlisin1
1 Department of Civil and Structural Engineering, Faculty of Engineering and Built Environment,Universiti Kebangsaan Malaysia, 43600 Bangin, Malaysia
2 Department of Chemical Engineering, Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia,43600 Bangin, Malaysia
3 Tasik Chini Reasearch Centre, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 Bangin, Malaysia
Correspondence should be addressed to Bieby Voijant Tangahu, [email protected]
Received 17 March 2011; Accepted 3 June 2011
Academic Editor: Hans-Jörg Bart
Copyright © 2011 Bieby Voijant Tangahu et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.
Heavy metals are among the most important sorts of contaminant in the environment. Several methods already used to cleanup the environment from these kinds of contaminants, but most of them are costly and difficult to get optimum results.Currently, phytoremediation is an effective and affordable technological solution used to extract or remove inactive metals andmetal pollutants from contaminated soil and water. This technology is environmental friendly and potentially cost effective. Thispaper aims to compile some information about heavy metals of arsenic, lead, and mercury (As, Pb, and Hg) sources, effectsand their treatment. It also reviews deeply about phytoremediation technology, including the heavy metal uptake mechanismsand several research studies associated about the topics. Additionally, it describes several sources and the effects of As, Pb, andHg on the environment, the advantages of this kind of technology for reducing them, and also heavy metal uptake mechanismsin phytoremediation technology as well as the factors affecting the uptake mechanisms. Some recommended plants which arecommonly used in phytoremediation and their capability to reduce the contaminant are also reported.
1. Introduction
Heavy metals are among the contaminants in the envi-ronment. Beside the natural activities, almost all humanactivities also have potential contribution to produce heavymetals as side effects. Migration of these contaminants intononcontaminated areas as dust or leachates through the soiland spreading of heavy metals containing sewage sludge are afew examples of events contributing towards contaminationof the ecosystems [1].
Several methods are already being used to clean up theenvironment from these kinds of contaminants, but most ofthem are costly and far away from their optimum perfor-mance. The chemical technologies generate large volumetricsludge and increase the costs [2]; chemical and thermalmethods are both technically difficult and expensive that allof these methods can also degrade the valuable component
of soils [3]. Conventionally, remediation of heavy-metal-contaminated soils involves either onsite management orexcavation and subsequent disposal to a landfill site. Thismethod of disposal solely shifts the contamination problemelsewhere along with the hazards associated with transporta-tion of contaminated soil and migration of contaminantsfrom landfill into an adjacent environment. Soil washingfor removing contaminated soil is an alternative way toexcavation and disposal to landfill. This method is very costyand produces a residue rich in heavy metals, which willrequire further treatment. Moreover, these physio-chemicaltechnologies used for soil remediation render the land usageas a medium for plant growth, as they remove all biologicalactivities [1].
Recent concerns regarding the environmental contami-nation have initiated the development of appropriate tech-nologies to assess the presence and mobility of metals in
-
2 International Journal of Chemical Engineering
soil [4], water, and wastewater. Presently, phytoremedia-tion has become an effective and affordable technologicalsolution used to extract or remove inactive metals andmetal pollutants from contaminated soil. Phytoremediationis the use of plants to clean up a contamination fromsoils, sediments, and water. This technology is environmentalfriendly and potentially costeffective. Plants with exceptionalmetal-accumulating capacity are known as hyperaccumu-lator plants [5]. Phytoremediation takes the advantage ofthe unique and selective uptake capabilities of plant rootsystems, together with the translocation, bioaccumulation,and contaminant degradation abilities of the entire plantbody [3].
Many species of plants have been successful in absorbingcontaminants such as lead, cadmium, chromium, arsenic,and various radionuclides from soils. One of phytoremedia-tion categories, phytoextraction, can be used to remove heavymetals from soil using its ability to uptake metals which areessential for plant growth (Fe, Mn, Zn, Cu, Mg, Mo, and Ni).Some metals with unknown biological function (Cd, Cr, Pb,Co, Ag, Se, Hg) can also be accumulated [5].
The objectives of this paper are to discuss the potentialof phytoremediation technique on treating heavy metal-contaminated side, to provide a brief view about heavymetals uptake mechanisms by plant, to give some descriptionabout the performance of several types of plants to uptakeheavy metals and to describe about the fate of heavy metalsin plant tissue, especially on arsenic (As), lead (Pb), andmercury (Hg). This study is related to a research project thataims to identify potential plants in tropical country such asMalaysia which can uptake heavy metal contaminants frompetrochemical wastewater.
2. Heavy Metals: Sources andEffect in the Environment
Heavy metals are conventionally defined as elements withmetallic properties and an atomic number >20. The mostcommon heavy metal contaminants are Cd, Cr, Cu, Hg, Pb,and Zn. Metals are natural components in soil [6]. Some ofthese metals are micronutrients necessary for plant growth,such as Zn, Cu, Mn, Ni, and Co, while others have unknownbiological function, such as Cd, Pb, and Hg [1].
Metal pollution has harmful effect on biological sys-tems and does not undergo biodegradation. Toxic heavymetals such as Pb, Co, Cd can be differentiated fromother pollutants, since they cannot be biodegraded but canbe accumulated in living organisms, thus causing variousdiseases and disorders even in relatively lower concentrations[7]. Heavy metals, with soil residence times of thousands ofyears, pose numerous health dangers to higher organisms.They are also known to have effect on plant growth, groundcover and have a negative impact on soil microflora [8]. It iswell known that heavy metals cannot be chemically degradedand need to be physically removed or be transformed intonontoxic compounds [1].
2.1. Arsenic (As). Arsenic (atomic number 33) is a silver-greybrittle crystalline solid with atomic weight of 74.9, specific
gravity 5.73, melting point 817◦C (at 28 atm), boiling point613◦C, and vapor pressure 1 mm Hg at 372◦C [9]. Arsenicis a semimetallic element with the chemical symbol “As”.Arsenic is odorless and tasteless. Arsenic can combine withother elements to form inorganic and organic arsenicals[10]. In the environment, arsenic is combined with oxygen,chlorine, and sulfur to form inorganic arsenic compounds.Inorganic arsenic compounds are mainly used to preservewood. Organic arsenic compounds are used as pesticides,primarily on cotton plants [11].
Arsenic exists in the −3, 0, +3, and +5 valence oxidationstates [9], and in a variety of chemical forms in natural watersand sediments [12]. Environmental forms include arseniousacids (H3AsO3, H3AsO3, H3AsO3
2−), arsenic acids (H3AsO4,H3AsO4
−, H3AsO42−), arsenites, arsenates, methylarsenicacid, dimethylarsinic acid, and arsine. Two most commonforms in natural waters arsenite (AsO3
3−) and inorganicarsenate (AsO4
3−), referred as As3+ and As5+ [9]. From boththe biological and the toxicological points of view, arseniccompounds can be classified into three major groups. Thesegroups are inorganic arsenic compounds, organic arseniccompounds, and arsine gas [13].
It is a hard acid and preferentially complexes with oxidesand nitrogen. Trivalent arsenites predominate in moderatelyreducing anaerobic environments such as groundwater [9].The most common trivalent inorganic arsenic compoundsare arsenic trioxide, sodium arsenite, and arsenic trichloride[13]. Trivalent (+3) arsenates include As(OH)3, As(OH)4
−,AsO2OH2−, and AsO33− [9]. Arsenite (As(OH)3, As3+) ispredominant in reduced redox potential conditions [12].
Arsenic is one of the contaminants found in the envi-ronment which is notoriously toxic to man and other livingorganisms [14]. It is a highly toxic element that existsin various species, and the toxicity of arsenic dependson its species. The pH, redox conditions, surroundingmineral composition, and microbial activities affect the form(inorganic or organic) and the oxidation state of arsenic.It is generally accepted that the inorganic species, arsenite[As3+] and arsenate [As5+], are the predominant species inmost environments, although the organic ones might also bepresent [15].
In general, inorganic compounds of arsenic are regardedas more highly toxic than most organic forms which are lesstoxic [10, 14, 16, 17]. The trivalent compounds (arsenites)are more toxic than the pentavalent compounds (arsenates)[16, 17]. It has been reported that As3+ is 4 to 10 timesmore soluble in water than As5+. However, the trivalentmethylated arsenic species have been found to be more toxicthan inorganic arsenic because they are more efficient atcausing DNA breakdown [17]. Although As5+ tends to beless toxic compared to of As3+, it is thermodynamically morestable due to it predominates under normal conditions andbecomes the cause of major contaminant in ground water[14]. Arsenate which is in the pentavalent state (As5+) is alsoconsidered to be toxic and carcinogenic to human [18].
2.2. Lead (Pb). Lead (Pb), with atomic number 82, atomicweight 207.19, and a specific gravity of 11.34, is a bluishor silvery-grey metal with a melting point of 327.5◦C and a
-
International Journal of Chemical Engineering 3
boiling point at atmospheric pressure of 1740◦C. It has fournaturally occurring isotopes with atomic weights 208, 206,207 and 204 (in decreasing order of abundance). Despitethe fact that lead has four electrons on its valence shell, itstypical oxidation state is +2 rather than +4, since only two ofthe four electrons ionize easily. Apart from nitrate, chlorate,and chloride, most of the inorganic salts of lead2+ have poorsolubility in water [19]. Lead (Pb) exists in many forms inthe natural sources throughout the world and is now one ofthe most widely and evenly distributed trace metals. Soil andplants can be contaminated by lead from car exhaust, dust,and gases from various industrial sources.
Pb2+ was found to be acute toxic to human beings whenpresent in high amounts. Since Pb2+ is not biodegradable,once soil has become contaminated, it remains a long-termsource of Pb2+ exposure. Metal pollution has a harmful effecton biological systems and does not undergo biodegradation[7].
Soil can be contaminated with Pb from several othersources such as industrial sites, from leaded fuels, old leadplumbing pipes, or even old orchard sites in productionwhere lead arsenate is used. Lead accumulates in the upper8 inches of the soil and is highly immobile. Contamination islong-term. Without remedial action, high soil lead levels willnever return to normal [20].
In the environment, lead is known to be toxic to plants,animals, and microorganisms. Effects are generally limited toespecially contaminated areas [21]. Pb contamination in theenvironment exists as an insoluble form, and the toxic metalspose serious human health problem, namely, brain damageand retardation [5].
2.3. Mercury (Hg). Mercury is a naturally occurring metalthat is present in several forms. Metallic mercury is shiny,silver-white, odorless liquid. Mercury combines with otherelements, such as chlorine, sulfur, or oxygen, to form inor-ganic mercury compounds or salts, which are usually whitepowders or crystals. Mercury also combines with carbon tomake organic mercury compounds [22]. Mercury, which hasthe lowest melting point (−39◦C) of all the pure metals,is the only pure metal that is liquid at room temperature.However, due to its several physical and chemical advantagessuch as its low boiling point (357◦C) and easy vaporization,mercury is still an important material in many industrialproducts [23]. As any other metal, mercury could occur inthe soil in various forms. It dissolves as free ion or solublecomplex and is nonspecifically adsorbed by binding mainlydue to the electrostatic forces, chelated, and precipitated assulphide, carbonate, hydroxide, and phosphate. There arethree soluble forms of Hg in the soil environment. The mostreduced is Hg0 metal with the other two forms being ionicof mercurous ion Hg2
2+ and mercuric ion Hg2+, in oxidizingconditions especially at low pH. Hg+ ion is not stable underenvironmental conditions since it dismutates into Hg0 andHg2+. A second potential route for the conversion of mercuryin the soil is methylation to methyl or dimethyl mercury byanaerobic bacteria [24].
Mercury is a persistent environmental pollutant withbioaccumulation ability in fish, animals, and human beings
[23]. Mercury salts and organomercury compounds areamong the most poisonous substances in our environment.The mechanism and extent of toxicity depend strongly on thetype of compound and the redox state of mercury [25].
Environmental contamination due to mercury is causedby several industries, petrochemicals, minings, painting, andalso by agricultural sources such as fertilizer and fungicidalsprays [26]. Some of the more common sources of mercuryfound throughout the environment include but may notbe limited to the household bleach, acid, and causticchemicals (e.g., battery acid, household lye, muriatic acid(hydrochloric acid), sodium hydroxide, and sulfuric acid),instrumentation containing mercury (e.g., medical instru-ments, thermometers, barometers, and manometers), dentalamalgam (fillings), latex paint (manufactured prior to 1990),batteries, electric lighting (fluorescent lamps, incandescentwire filaments, mercury vapor lamps, ultraviolet lamps),pesticides, pharmaceuticals (e.g., nasal sprays, cosmetics,contact lens products), household detergents and cleaners,laboratory chemicals, inks and paper coatings, lubricationoils, wiring devices and switches, and textiles. Thoughmercury use in many of the above items being produced nowis restricted or banned, there are still some existing, olderproducts in use [22].
Terrestrial plants are generally insensitive to the harmfuleffects of mercury compounds; however, mercury is knownto affect photosynthesis and oxidative metabolism by inter-fering with electron transport in chloroplasts and mitochon-dria. Mercury also inhibits the activity of aquaporins andreduces plant water uptake [27].
Mercury and its compounds are cumulative toxins and insmall quantities are hazardous to human health. The majoreffects of mercury poisoning manifest as neurological andrenal disturbances as it can easily pass the blood-brain barrierand has effect on the brain [26].
3. Phytoremediation Technology
Phytoremediation techniques have been briefly depictedin many literatures or articles. The generic term “phy-toremediation” consists of the Greek prefix phyto (plant),attached to the Latin root remedium (to correct or removean evil) [28, 29]. Some definitions on phytoremediationthat have been described by several researchers are listed inTable 1.
Generally, according to the above researchers, phytore-mediation is defined as an emerging technology usingselected plants to clean up the contaminated environmentfrom hazardous contaminant to improve the environmentquality. Figure 1 depicts the uptake mechanisms of bothorganics and inorganics contaminants through phytore-mediation technology. For organics, it involves phytosta-bilization, rhizodegradation, rhizofiltration, phytodegrada-tion, and phytovolatilization. These mechanisms related toorganic contaminant property are not able to be absorbedinto the plant tissue. For inorganics, mechanisms which canbe involved are phytostabilization, rhizofiltration, phytoac-cumulation and phytovolatilization.
-
4 International Journal of Chemical Engineering
Table 1: Definition of phytoremediation.
No. Researchers Definition of phytoremediation
(1) [30] The use of plants to improve degraded environments
(2) [31]The use of plants, including trees and grasses, to remove, destroy or sequester hazardous contaminants frommedia such as air, water, and soil
(3) [24]The use of plants to remediate toxic chemicals found in contaminated soil, sludge, sediment, ground water,surface water, and wastewater
(4) [32]An emerging technology using specially selected and engineered metal accumulating plants forenvironmental cleanup
(5) [33] The use of vascular plants to remove pollutants from the environment or to render them harmless
(6) [3]
The engineered use of green plant to remove, contain, or render harmless such environmental contaminantsas heavy metals, trace elements, organic compounds, and radioactive compounds in soil or water. Thisdefinition includes all plant-influenced biological, chemical, and physical processes that aid in the uptake,sequestration, degradation, and metabolism of contaminants, either by plants or by the free-living organismsthat constitute the plant rhizosphere
(7) [29]Phytoremediation is the name given to a set of technologies that use different plants as a containment,destruction, or an extraction technique. Phytoremediation is an emerging technology that uses variousplants to degrade, extract, contain, or immobilize contaminants from soil and water
(8) [34]Phytoremediation in general implies the use of plants (in combination with their associatedmicroorganisms) to remove, degrade, or stabilize contaminants
Organiccontaminants
Medium Inorganiccontaminants
Remediatedcontaminant
Phytovolatilization Atmosphere Phytovolatilization
Remediatedcontaminant
Phytodegradation Plant PhytoaccumulationPhytoextraction
RhizofiltrationRhizofiltration
Rhizodegradation
Phytostabilization
SoilPhytostabilization
Contaminated media
Figure 1: Uptake mechanisms on phytoremediation technology. Source: [35].
Based on Figure 1, some certain essential processesinvolved in phytoremediation technology [29, 31] are phy-tostabilization and phytoextraction for inorganic contami-nants, and phytotransformation/phytodegradation, rhizofil-tration, and rhizodegradation for organic contaminants.
The root plants exudates to stabilize, demobilize andbind the contaminants in the soil matrix, thereby reducingtheir bioavailability. These all are called as phytostabilizationprocess. Certain plant species have used to immobilizecontaminants in the soil and ground water through absorp-tion and accumulation by roots, adsorption onto roots,or precipitation within the root zone. This process is fororganics and metals contaminants in soils, sediments, andsludges medium [29, 31].
Specific plant species can absorb and hyperaccumulatemetal contaminants and/or excess nutrients in harvestableroot and shoot tissue, from the growth substrate through
phytoextraction process. This is for metals, metalloids,radionuclides, nonmetals, and organics contaminants insoils, sediments, and sludges medium [29, 31].
Phytovolatilization process is the plants ability toabsorb and subsequently volatilize the contaminant intothe atmosphere. This process is for metal contaminantsin groundwater, soils, sediments, and sludges medium.Since phytotransformation/phytodegradation process is thebreakdown of contaminants taken up by plants throughmetabolic processes within the plant or the breakdown ofcontaminants externally to the plant through the effect ofcompounds produced by the plants. This process is forcomplex organic molecules that are degraded into simplermolecule contaminants in soils, sediments, sludges, andgroundwater medium [29, 31].
Plant roots take up metal contaminants and/or excessnutrients from growth substrates through rhizofiltration
-
International Journal of Chemical Engineering 5
(=root) process, the adsorption, or, precipitation onto plantroots or absorption into the roots of contaminants that arein solution surrounding the root zone. This process is formetals, excess nutrients, and radionuclide contaminants ingroundwater, surface water, and wastewater medium [29,31].
The breakdown of contaminants in the soil throughmicrobial activity that is enhanced by the presence of theroot zone is called rhizodegradation. This process usesmicroorganisms to consume and digest organic substancesfor nutrition and energy. Natural substances released bythe plant roots, sugars, alcohols, and acids, contain organiccarbon that provides food for soil microorganisms andestablish a dense root mass that takes up large quantities ofwater. This process is for organic substance contaminants insoil medium [29, 31].
4. Mechanisms of Heavy Metal Uptake by Plant
Contaminant uptake by plants and its mechanisms havebeen being explored by several researchers. It could beused to optimize the factors to improve the performanceof plant uptake. According to Sinha et al. [36], the plantsact both as “accumulators” and “excluders”. Accumulatorssurvive despite concentrating contaminants in their aerialtissues. They biodegrade or biotransform the contaminantsinto inert forms in their tissues. The excluders restrictcontaminant uptake into their biomass.
Plants have evolved highly specific and very efficientmechanisms to obtain essential micronutrients from theenvironment, even when present at low ppm levels. Plantroots, aided by plant-produced chelating agents and plant-induced pH changes and redox reactions, are able tosolubilize and take up micronutrients from very low levelsin the soil, even from nearly insoluble precipitates. Plantshave also evolved highly specific mechanisms to translocateand store micronutrients. These same mechanisms arealso involved in the uptake, translocation, and storage oftoxic elements, whose chemical properties simulate those ofessential elements. Thus, micronutrient uptake mechanismsare of great interest to phytoremediation [37].
The range of known transport mechanisms or specializedproteins embedded in the plant cell plasma membraneinvolved in ion uptake and translocation include (1) pro-ton pumps (′′-ATPases that consume energy and generateelectrochemical gradients), (2) co- and antitransporters(proteins that use the electrochemical gradients generatedby ′′-ATPases to drive the active uptake of ions), and (3)channels (proteins that facilitate the transport of ions intothe cell). Each transport mechanism is likely to take up arange of ions. A basic problem is the interaction of ionicspecies during uptake of various heavy metal contaminants.After uptake by roots, translocation into shoots is desirablebecause the harvest of root biomass is generally not feasible.Little is known regarding the forms in which metal ions aretransported from the roots to the shoots [37].
Plant uptake-translocation mechanisms are likely to beclosely regulated. Plants generally do not accumulate traceelements beyond near-term metabolic needs. And these
requirements are small ranging from 10 to 15 ppm of mosttrace elements suffice for most needs [37]. The exceptionsare “hyperaccumulator” plants, which can take up toxicmetal ions at levels in the thousands of ppm. Anotherissue is the form in which toxic metal ions are stored inplants, particularly in hyperaccumulating plants, and howthese plants avoid metal toxicity. Multiple mechanisms areinvolved. Storage in the vacuole appears to be a major one[37].
Water, evaporating from plant leaves, serves as a pump toabsorb nutrients and other soil substances into plant roots.This process, termed evapotranspiration, is responsible formoving contamination into the plant shoots as well. Sincecontamination is translocated from roots to the shoots,which are harvested, contamination is removed while leavingthe original soil undisturbed. Some plants that are usedin phytoextraction strategies are termed “hyperaccumula-tors.” They are plants that achieve a shoot-to-root metal-concentration ratio greater than one. Nonaccumulatingplants typically have a shoot-to-root ratio considerablyless than one. Ideally, hyperaccumulators should thrive intoxic environments, require little maintenance and producehigh biomass, although few plants perfectly fulfill theserequirements [38].
Metal accumulating plant species can concentrate heavymetals like Cd, Zn, Co, Mn, Ni, and Pb up to 100 or1000 times those taken up by nonaccumulator (excluder)plants. In most cases, microorganisms bacteria and fungi,living in the rhizosphere closely associated with plants, maycontribute to mobilize metal ions, increasing the bioavailablefraction. Their role in eliminating organic contaminantsis even more significant than that in case of inorganiccompounds [39, 40].
Heavy metal uptake by plant through phytoremediationtechnologies is using these mechanisms of phytoextraction,phytostabilisation, rhizofiltration, and phytovolatilization asshown in Figure 2.
4.1. Phytoextraction. Phytoextraction is the uptake/absorp-tion and translocation of contaminants by plant roots intothe above ground portions of the plants (shoots) that can beharvested and burned gaining energy and recycling the metalfrom the ash [28, 39–42].
4.2. Phytostabilisation. Phytostabilisation is the use of certainplant species to immobilize the contaminants in the soil andgroundwater through absorption and accumulation in planttissues, adsorption onto roots, or precipitation within theroot zone preventing their migration in soil, as well as theirmovement by erosion and deflation [28, 39–42].
4.3. Rhizofiltration. Rhizofiltration is the adsorption orprecipitation onto plant roots or absorption into andsequesterization in the roots of contaminants that are insolution surrounding the root zone by constructed wetlandfor cleaning up communal wastewater [28, 39–42].
4.4. Phytovolatilization. Phytovolatilization is the uptake andtranspiration of a contaminant by a plant, with release ofthe contaminant or a modified form of the contaminant to
-
6 International Journal of Chemical Engineering
Phytoaccumulation/phytoextraction
Phytovolatilization
Phytodegradation
Rhizodegradation
Contaminants uptake
Phytostabilization
Figure 2: The mechanisms of heavy metals uptake by plant through phytoremediation technology.
the atmosphere from the plant. Phytovolatilization occurs asgrowing trees and other plants take up water along with thecontaminants. Some of these contaminants can pass throughthe plants to the leaves and volatilize into the atmosphere atcomparatively low concentrations [28, 39–42].
Plants also perform an important secondary role in phys-ically stabilizing the soil with their root system, preventingerosion, protecting the soil surface, and reducing the impactof rain. At the same time, plant roots release nutrientsthat sustain a rich microbial community in the rhizosphere.Bacterial community composition in the rhizosphere isaffected by complex interactions between soil type, plantspecies, and root zone location. Microbial populations aregenerally higher in the rhizosphere than in the root-freesoil. This is due to a symbiotic relationship between soilmicroorganisms and plants. This symbiotic relationship canenhance some bioremediation processes. Plant roots alsomay provide surfaces for sorption or precipitation of metalcontaminants [27].
In phytoremediation, the root zone is of special interest.The contaminants can be absorbed by the root to be subse-quently stored or metabolised by the plant. Degradation ofcontaminants in the soil by plant enzymes exuded from theroots is another phytoremediation mechanism [43].
For many contaminants, passive uptake via micropores inthe root cell walls may be a major route into the root, wheredegradation can take place [3].
5. Factors Affecting the Uptake Mechanisms
There are several factors which can affect the uptakemechanism of heavy metals, as shown in Figure 3. By havingknowledge about these factors, the uptake performance byplant can be greatly improved.
5.1. The Plant Species. Plants species or varieties arescreened, and those with superior remediation propertiesare selected [31]. The uptake of a compound is affectedby plant species characteristic [44]. The success of thephytoextraction technique depends upon the identificationof suitable plant species that hyperaccumulate heavy metalsand produce large amounts of biomass using established cropproduction and management practices [24].
5.2. Properties of Medium. Agronomical practices are devel-oped to enhance remediation (pH adjustment, addition ofchelators, fertilizers) [31]. For example, the amount of leadabsorbed by plants is affected by the pH, organic matter, and
-
International Journal of Chemical Engineering 7
Plantspecies
Propertiesof medium
Root zone
Environmentalcondition
Chemicalproperties
of thecontaminant
Bioavailabilityof themetal
Chelatingagentadded
Uptakemechanisms
Figure 3: Factors which are affecting the uptake mechanisms ofheavy metals.
the phosphorus content of the soil. To reduce lead uptake byplants, the pH of the soil is adjusted with lime to a level of 6.5to 7.0 [20].
5.3. The Root Zone. The Root Zone is of special interestin phytoremediation. It can absorb contaminants and storeor metabolize it inside the plant tissue. Degradation ofcontaminants in the soil by plant enzymes exuded from theroots is another phytoremediation mechanism. A morpho-logical adaptation to drought stress is an increase in rootdiameter and reduced root elongation as a response to lesspermeability of the dried soil [43].
5.4. Vegetative Uptake. Vegetative Uptake is affected by theenvironmental conditions [44]. The temperature affectsgrowth substances and consequently root length. Rootstructure under field conditions differs from that undergreenhouse condition [43]. The success of phytoremediation,more specifically phytoextraction, depends on a contami-nant-specific hyperaccumulator [45]. Understanding massbalance analyses and the metabolic fate of pollutants in plantsare the keys to proving the applicability of phytoremediation[46].
Metal uptake by plants depends on the bioavailability ofthe metal in the water phase, which in turn depends on theretention time of the metal, as well as the interaction withother elements and substances in the water. Furthermore,when metals have been bound to the soil, the pH, redoxpotential, and organic matter content will all affect the ten-dency of the metal to exist in ionic and plant-available form.Plants will affect the soil through their ability to lower the pHand oxygenate the sediment, which affects the availability ofthe metals [47], increasing the bioavailability of heavy metals
by the addition of biodegradable physicochemical factors,such as chelating agents and micronutrients [34].
5.5. Addition of Chelating Agent. The increase of the uptakeof heavy metals by the energy crops can be influencedby increasing the bioavailability of heavy metals throughaddition of biodegradable physicochemical factors such aschelating agents, and micronutrients, and also by stimulatingthe heavy-metal-uptake capacity of the microbial commu-nity in and around the plant. This faster uptake of heavymetals will result in shorter and, therefore, less expensiveremediation periods. However, with the use of syntheticchelating agents, the risk of increased leaching must betaken into account [34]. The use of chelating agents inheavy-metal-contaminated soils could promote leaching ofthe contaminants into the soil. Since the bioavailability ofheavy metals in soils decreases above pH 5.5–6, the use of achelating agent is warranted, and may be required, in alkalinesoils. It was found that exposing plants to EDTA for a longerperiod (2 weeks) could improve metal translocation in planttissue as well as the overall phytoextraction performance.The application of a synthetic chelating agent (EDTA) at5 mmol/kg yielded positive results [8]. Plant roots exudeorganic acids such as citrate and oxalate, which affect thebioavailability of metals. In chelate-assisted phytoremedi-ation, synthetic chelating agents such as NTA and EDTAare added to enhance the phytoextraction of soil-pollutingheavy metals. The presence of a ligand affects the biouptakeof heavy metals through the formation of metal-ligandcomplexes and changes the potential to leach metals belowthe root zone [48].
6. Effectiveness of Heavy MetalsUptake by Plants
Several studies have described the performance of heavymetals uptake by plants. It is reported that phytoreme-diation technology is an alternative to treat heavy-metal-contaminated side which will be more admitted in order toremediate the environment. Table 2 lists some research doneto remediate heavy metals from contaminated soil, whileTable 3 lists some research conducted to remediate themfrom contaminated water and wastewater.
Based on the collected data from the phytoremediationresearch listed in Tables 2 and 3, the accumulation of heavymetals As, Pb, and Hg in plant tissue is summarized inrespective, Figures 4, 5, and 6.
According to Figure 4, the highest accumulation of As inplant tissue (the researchers have not detailed which part itis, but it might be the whole plant) occurs in Pteris vittataL. species. It can reach more than 0.7 mg As/g dry weightof plant. In plant root, the highest accumulation of As is inPopulus nigra, which can reach more than 0.2 mg As/g dryweight of plant root.
As can be seen in Figure 5, several plants could accumu-late Pb in their tissue of more than 50 mg/g dry weight ofplant. Among those species are species of Brassica campestrisL, Brassica carinata A. Br., Brassica juncea (L.) Czern. and
-
8 International Journal of Chemical Engineering
Ta
ble
2:P
hyto
rem
edia
tion
stu
dyon
soil
med
ium
.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(1)
[16]
Gre
enh
ouse
pot
exp
erim
ent
(6,1
0,an
d16
days
)
Phy
toex
trac
tion
(soi
lw
asad
ded
toaq
ueo
us
solu
tion
and
was
drie
dov
ern
igh
tin
anov
enat
120◦
C,c
oole
d,an
dtr
ansf
erre
dto
the
pot)
Aqu
eou
sso
luti
onco
nta
inin
g0.
1041
gof
sodi
um
arse
nat
eh
epta
hydr
ate
(Na 2
HA
sO4·7
H2O
),th
em
ixtu
rew
hic
hco
nta
ined
50m
g/kg
ofA
s(w
etw
eigh
t)
Leer
sia
oryz
oide
s(r
ice-
cut
gras
s)—
terr
estr
ialp
lan
t
Th
ein
crea
sein
plan
tsi
zeis
mat
ched
bya
decr
ease
insh
oot
arse
nic
con
cen
trat
ion
.T
he
data
show
that
12,1
3,an
d13
mg/
m2
ofar
sen
icw
ere
abso
rbed
byth
esh
oots
at6,
10,a
nd
16w
eeks
,res
pec
tive
ly.S
ince
the
SRQ
and
PE
Cs
alle
xhib
itth
esa
me
dow
nwar
dtr
end
afte
r6
wk,
itis
sugg
este
dth
atpe
riod
icm
owin
gof
Leer
sia
oryz
oide
sgr
own
for
phyt
oext
ract
ion
purp
oses
onco
nta
min
ated
lan
dco
uld
mai
nta
inth
eh
igh
arse
nic
upt
ake
at6
wee
k.
(2)
[33]
Labo
rato
ry(p
otex
peri
men
t)(9
0da
ys)
Fly
ash
and
soil
mix
ture
s
Pb
asle
adn
itra
te,Z
nas
zin
csu
lfat
e,N
ias
nic
kel
sulf
ate,
Mn
asm
anga
nes
ech
lori
de,a
nd
Cu
asco
pper
sulf
ate
(100
0pp
mco
nce
ntr
atio
nea
ch(S
pike
d))
Scir
pus
litto
ralis
—se
mia
quat
ic
Th
em
etal
con
ten
tra
tios
BO
/soi
l(B
/S)
wer
eh
igh
erth
ansh
oot/
soil
rati
os(T
/S)
for
allt
he
met
als,
the
hig
hes
tbe
ing
for
Ni.
Met
alra
tios
BO
/wat
er(B
/W)
wer
eal
soh
igh
erth
ansh
oot/
wat
er(T
/W)
rati
os,b
ut
the
B/W
rati
ow
asm
axim
um
for
Zn
.All
the
met
als
exce
ptN
ish
owed
neg
ativ
eco
rrel
atio
nw
ith
nit
roge
nbu
tth
eyw
ere
alln
onsi
gnifi
can
t.H
owev
er,P
upt
ake
show
edpo
siti
veco
rrel
atio
ns
wit
hal
lth
em
etal
s,an
dal
lwer
esi
gnifi
can
tat
1%co
nfi
den
celim
it.
(3)
[49]
Fiel
dst
udy
(90
days
)So
il(a
gric
ult
ura
llan
dar
ea)
(Cu
,Cd,
Cr,
Zn
,Fe,
Ni,
Mn
,an
dP
b)
Wh
eat
(Tri
ticu
mae
stiv
umL.
)—te
rres
tria
lIn
dian
mu
star
d(B
rass
ica
cam
pest
ris
L.)—
terr
estr
ial
An
alys
esof
efflu
ents
and
soil
sam
ples
hav
esh
own
hig
hm
etal
con
ten
tth
anth
epe
rmis
sibl
elim
itex
cept
Pb.
An
alys
esof
plan
tsa
mpl
esh
ave
indi
cate
dth
em
axim
um
accu
mu
lati
onof
Fefo
llow
edby
Mn
and
Zn
inro
ot>
shoo
t>le
aves>
seed
s.M
axim
um
incr
ease
inph
otos
ynth
etic
pigm
ent
was
obse
rved
betw
een
30an
d60
days
wh
ilepr
otei
nco
nte
nt
was
fou
nd
max
imu
mbe
twee
n60
and
90da
ysof
grow
thpe
riod
inbo
thpl
ants
.
-
International Journal of Chemical Engineering 9
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(4)
[5]
Labo
rato
ry(6
5da
ys)
Phy
toex
trac
tion
(soi
l)P
bby
usi
ng
stan
dard
Pb
solu
tion
s(7
5m
gP
b/1
kgso
il)
Cre
epin
gzi
nn
ia(A
lter
nant
hera
phyl
oxer
oide
s)—
aqu
atic
Mos
sro
se(S
anvi
talia
proc
umbe
ns)—
terr
estr
ial
Alli
gato
rw
eed
(Por
tula
cagr
andi
flora
)—aq
uat
ic
Alt
erna
nthe
raph
ylox
eroi
des
show
sth
eh
igh
est
lead
con
ten
tin
its
tiss
ues
.Th
ism
igh
tbe
cau
sed
byit
form
ing
lon
gst
olon
s,a
mas
sive
fibr
ous
root
syst
em,
and
larg
esu
rfac
ear
eaw
hic
hbe
nefi
tsth
eac
cum
ula
tion
ofle
ad.E
ffici
ency
proc
ess
30–8
0%.
(5)
[34]
Lite
ratu
rere
view
Soil
Cd,
Cr,
Cu
,Ni,
Pb,
and
Zn
Bra
ssic
aju
ncea
(In
dian
mu
star
d),B
rass
ica
rapa
(fiel
dm
ust
ard)
,an
dB
rass
ica
napu
s(r
ape)
—te
rres
tria
l
Bra
ssic
ara
paex
hib
ited
the
hig
hes
taffi
nit
yfo
rac
cum
ula
tin
gC
dan
dP
bfr
omth
eso
il,ei
ther
wit
h/w
ith
out
addi
tion
alu
seof
mob
ilizi
ng
soil
amen
dmen
ts.T
wo
Bra
ssic
asp
ecie
s(B
rass
ica
napu
san
dR
apha
nus
sati
vus)
wer
em
oder
atel
yto
lera
nt
wh
engr
own
ona
mu
lti-
met
alco
nta
min
ated
soil.
Th
edi
stri
buti
onof
hea
vym
etal
sin
the
orga
ns
ofcr
ops
decr
ease
din
the
follo
win
gor
der:
leav
es>
stem
s>ro
ots>
fru
itsh
ell>
seed
s.
(6)
[50]
Lab
orat
ory—
pot
exp
erim
ent
(12
days
)
Agr
opea
tan
dh
alf
stre
ngt
hH
oagl
and
solu
tion
Ars
enic
(As)
asof
sodi
um
(met
a-)
arse
nit
e(5
0u
M,1
50u
Man
d30
0u
M)
Bra
ssic
aju
ncea
var.
Var
un
aan
dP
usa
Bol
d—te
rres
tria
l
Incr
ease
/dec
reas
eof
anti
oxid
ant
enzy
mes
acti
viti
essh
owed
not
mu
chch
ange
sat
the
give
nco
nce
ntr
atio
ns.
Th
eda
tapr
esen
ted
indi
cate
sth
edi
ffer
enti
alre
spon
ses
inbo
thth
eva
riet
ies
and
also
that
the
incr
ease
dto
lera
nce
inP.
Bol
dm
aybe
due
toth
ede
fen
sive
role
ofan
tiox
idan
ten
zym
es,i
ndu
ctio
nof
MA
PK
,an
du
preg
ula
tion
ofP
CS
tran
scri
ptw
hic
his
resp
onsi
ble
for
the
prod
uct
ion
ofm
etal
-bin
din
gpe
ptid
es.
-
10 International Journal of Chemical Engineering
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(7)
[51]
Fiel
dst
udy
(tri
als
toex
trac
th
eavy
met
als
from
two
con
tam
inat
edso
ils,o
ne
calc
areo
us
(5ye
ars)
and
one
acid
ic(2
year
s))
Phy
toex
trac
tion
(soi
l)C
dan
dZ
nW
illow
(Sal
ixvi
min
alis
)—te
rres
tria
l
Salix
had
perf
orm
edbe
tter
onth
eac
idic
soil
beca
use
ofla
rger
biom
ass
prod
uct
ion
and
hig
her
met
alco
nce
ntr
atio
ns
insh
oots
.Add
itio
nof
elem
enta
lsu
lphu
rto
the
soil
did
not
yiel
dan
yad
diti
onal
ben
efit
inth
elo
ng
term
,bu
tap
plic
atio
nof
anFe
chel
ate
impr
oved
the
biom
ass
prod
uct
ion
.Cd
and
Zn
con
cen
trat
ion
sw
ere
sign
ifica
ntl
yh
igh
erin
leav
esth
anst
ems.
On
both
soils
,con
cen
trat
ion
insh
oots
decr
ease
dw
ith
tim
e.
(8)
[52]
Labo
rato
ry(2
6da
ys)
Slu
dge-
amen
ded
soils
Cd
and
Zn
Rap
hanu
ssa
tivu
sL.
Th
isst
udy
has
show
nth
atcl
ear
evid
ence
ofas
ludg
e-dr
iven
plat
eau
resp
onse
inm
etal
upt
ake
bypl
ants
will
only
beob
tain
edw
hen
stu
dies
hav
efo
un
da
good
hype
rbol
icre
lati
onsh
ipbe
twee
nso
ilso
luti
onm
etal
con
cen
trat
ion
wit
hin
crea
sin
gsl
udg
eap
plic
atio
nra
tean
dca
nlin
kth
isto
apl
atea
ure
spon
sein
plan
tu
ptak
eof
met
als.
-
International Journal of Chemical Engineering 11
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
Labo
rato
ry—
lysi
met
erpo
t(M
arch
1995
–Sep
tem
ber
1995
)So
il
Zn
asZ
nSO
4(5
0,1,
500,
2,00
0µ
g/g
(ppm
)Z
n.
and
2,00
0µ
g/g
(ppm
),an
d0µ
g/g
(ppm
)(c
ontr
ol)
rece
ived
nu
trie
nt
only
)
Hyb
rid
popl
ar(P
opul
ussp
.)—
terr
estr
ial
At
leve
lsof
zin
cab
ove
1,00
0µ
g/g
(ppm
)in
nu
trie
nt
adde
d,le
ach
ate
leve
lsw
ere
alw
ays
belo
w10
0µ
g/g
(ppm
)in
sam
ples
asth
ezi
nc
addi
tion
;th
ese
leve
lsin
crea
sed
the
follo
win
gda
yan
dth
ende
crea
sed
shar
ply
the
seco
nd
day
afte
rth
ezi
nc
addi
tion
,to
con
cen
trat
ion
sle
ssth
an10
0µ
g/g
(ppm
).T
he
zin
cco
nce
ntr
atio
nst
eadi
lyde
crea
sed
asth
epl
ants
appa
ren
tly
reab
sorb
edth
ezi
nc
asth
en
utr
ien
tw
ascy
cled
thro
ugh
the
pots
onsu
bseq
uen
tda
ys.T
he
root
tiss
ues
show
edm
uch
hig
her
con
cen
trat
ion
sof
accu
mu
late
dan
dse
ques
tere
dm
etal
than
did
the
abov
egr
oun
dpa
rts.
(9)
[3]
Labo
rato
ry(A
pril
1996
,2
mon
ths)
Soil
Zn
(160
µg/
gZ
n,
600µ
g/g
Zn
,an
d0µ
g/g
Zn
(con
trol
))
Eas
tern
gam
agra
ss(T
rips
acum
dact
yloi
des)
—te
rres
tria
l
Leac
hat
ean
alys
esfo
rzi
nc
indi
cate
that
init
ially
plan
tssu
bjec
ted
tobo
thle
vels
ofzi
nc
wer
ere
mov
ing
up
to70
%of
the
zin
cfr
omth
ele
ach
ate.
Th
epl
ants
rece
ivin
g16
0µ
g/g
Zn
had
grow
nco
nsi
dera
bly
and
wer
eal
mos
tth
esa
me
size
asth
eco
ntr
ols
(no
zin
c),b
ut
som
eof
the
mat
ure
leaf
blad
esw
ere
rolle
d;th
em
ean
zin
cre
mov
alra
tefo
rth
ese
plan
tsw
as50
%of
the
zin
cin
the
leac
hat
e.T
he
plan
tsre
ceiv
ing
600µ
g/g
Zn
wer
esm
alle
rth
anth
eco
ntr
ols,
thei
rco
lor
was
ada
rker
gree
n,m
ost
ofth
em
atu
rele
afbl
ades
wer
ero
lled,
and
the
mea
nzi
nc
rem
oval
rate
was
abou
t30
%of
the
zin
cin
the
leac
hat
e.
Soil
Pb
and
As
(up
to10
00µ
g/g
Pb
and
up
to20
0µ
g/g
As)
Hyb
rid
will
ow(S
alix
sp.)
and
hybr
idpo
plar
(Pop
ulus
sp.)
—te
rres
tria
l
Th
ew
illow
sw
ere
able
tore
mov
eap
prox
imat
ely
9.5%
ofth
eav
aila
ble
lead
and
abou
t1%
ofth
eto
tala
rsen
icfr
omth
eco
nta
min
ated
soil.
Th
ele
ssm
atu
rep
opla
rsre
mov
edab
out
1%of
the
avai
labl
ele
adan
d0.
1%of
the
tota
lars
enic
from
the
sam
eso
il.In
the
san
dex
peri
men
t,th
ew
illow
sto
oku
pab
out
40%
ofth
ead
min
iste
red
lead
and
30to
40%
ofth
ead
min
iste
red
arse
nic
.
-
12 International Journal of Chemical Engineering
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(10)
[53]
Fiel
d(1
976–
2001
)(S
oil)
Non
esse
nti
al(C
d,N
i,P
b)an
des
sen
tial
hea
vym
etal
s(C
u,F
e,M
n,Z
n).
Th
ete
tras
odiu
msa
ltof
ED
TAw
asap
plie
dat
rate
sof
0,0.
5,1,
2g
ED
TAsa
lt/k
gsu
rfac
e(2
5cm
dept
h)
soil
Sun
flow
er(H
elia
nthu
san
nuus
L.)
and
Hyb
rid
popl
ar(P
opul
usde
ltoi
des
Mar
sh.x
P.ni
gra
L.)—
terr
estr
ial
For
sun
flow
er,t
he
1.0
g/kg
rate
ofch
elat
ead
diti
onre
sult
edin
max
imal
rem
oval
ofth
eth
ree
non
esse
nti
alh
eavy
met
als
(Cd,
Ni,
Pb)
.Upt
ake
ofth
ees
sen
tial
hea
vym
etal
sby
sun
flow
erw
aslit
tle
affec
ted
byth
eE
DTA
.Th
ele
aves
ofsu
nfl
ower
grow
nw
ith
1.0
gE
DTA
Na 4·2
H2O
/kg
soil
accu
mu
late
dm
ore
Cd,
Ni,
and
Pb
than
leav
esof
sun
flow
ergr
own
wit
hou
tth
eE
DTA
salt
.Rem
oval
ofth
en
on-e
ssen
tial
hea
vym
etal
sby
sun
flow
erw
asgr
eate
rat
the
hig
her
plan
tde
nsi
tyco
mpa
red
toth
elo
wer
one.
(11)
[54]
Labo
rato
ry
18di
ffer
ent
phyt
orem
edat
ion
trea
tmen
ts.I
.par
cel:
min
ew
aste
wit
hou
tfl
yas
h.C
ontr
olan
du
ntr
eate
dpl
ot.3
test
plan
ts.I
I.m
ine
was
te+
fly
ash
wit
hou
tlim
ing.
Con
trol
and
un
trea
ted
plot
.3te
stpl
ants
.III
.m
ine
was
te+
fly
ash
+lim
ing.
Con
trol
and
un
trea
ted
plot
.3te
stpl
ants
.
As,
Cd,
Mo,
Pb,
Zn
(soi
l)an
dA
s,C
d,P
b,N
i,Z
n(w
ater
)
Gra
sses
(mix
ture
ofse
lect
edsp
ecie
s),s
orgh
um
(Sor
ghum
bico
lor
L.)
and
Suda
ngr
ass
(Sor
ghum
suda
nens
e)—
terr
estr
ial
Th
ech
emic
alri
sks
ofth
eG
yön
gyös
oros
zisp
oils
wer
eas
sess
ed.T
he
maj
orco
nta
min
ants
ofth
ew
aste
min
ew
ere
iden
tifi
ed:P
b,Z
n,C
d,A
s.T
he
con
cept
ofth
ein
tegr
ated
phyt
orem
edia
tion
was
succ
essf
ully
appl
ied
tove
geta
teG
yön
gyös
oros
zisp
oil.
Th
ebi
omas
spr
odu
ctio
nw
asdi
ffer
ent,
depe
ndi
ng
onth
ete
chn
olog
yva
rian
t.T
he
hig
hes
tbi
omas
spr
odu
ctio
nw
asac
hie
ved,
wh
enm
ult
ileve
lrev
ital
izat
ion
was
also
appl
ied.
Th
ein
tegr
ated
phyt
orem
edia
tion
trea
tmen
tsn
oton
lypr
odu
ced
hig
hbi
omas
s,bu
tal
sode
crea
sed
the
hea
vym
etal
con
ten
tin
the
plan
ts.
-
International Journal of Chemical Engineering 13
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(12)
[55]
Fiel
d(1
995–
1997
)So
ilN
i,C
u,C
d,Z
nW
illow
(Sal
ixsp
p.)—
terr
estr
ial
On
egr
oup
ofw
illow
had
rela
tive
lylo
wN
ian
dC
uin
the
bark
and
hig
hC
dan
dZ
nin
the
woo
d,w
ith
ago
odsu
rviv
alra
tean
dbi
omas
spr
odu
ctio
n.T
he
seco
nd
grou
pof
will
owh
adre
lati
vely
hig
hN
ian
dC
uin
the
bark
and
low
Cd
and
Zn
inth
ew
ood
and
per
form
edpo
orly
inte
rms
ofsu
rviv
alan
dbi
omas
spr
odu
ctio
n.
(13)
[8]
Labo
rato
ry(1
5M
ayan
d25
Sept
embe
r20
02)
Phy
toex
trac
tion
(soi
l)C
u,P
b,Z
n
Fesc
ue
(Fes
tuca
arun
dina
cea
Sch
reb.
),In
dian
mu
star
d(B
rass
ica
junc
ea(L
.)C
zern
.),a
nd
will
ow(S
alix
vim
inal
isL.
)—te
rres
tria
l
Th
eu
seof
the
free
acid
form
ofE
DTA
and
exp
osu
reti
me
ofon
eto
two
wee
ksbe
fore
har
vest
ing
incr
ease
dth
eco
nce
ntr
atio
nof
met
als
tran
sloc
ated
topl
ant
tiss
ues
.It
isfo
un
dn
osi
gnifi
can
tdi
ffer
ence
inh
eavy
met
alco
nce
ntr
atio
ns
inh
igh
eran
dlo
wer
soil
hor
izon
sbe
twee
nE
DTA
trea
ted
and
un
trea
ted
soils
.Exp
osin
gpl
ants
toE
DTA
for
alo
nge
rpe
riod
(2w
eeks
)co
uld
impr
ove
met
altr
ansl
ocat
ion
inpl
ant
tiss
ue
asw
ella
sth
eov
eral
lphy
toex
trac
tion
per
form
ance
.
(14)
[24]
Fiel
dex
per
imen
t(3
year
s)P
hyto
extr
acti
on(s
oil
con
ten
tw
ith
Hg)
Hg
(mea
nH
gco
nte
nt
ofth
eso
ilw
as29
.17µ
g/g
for
the
0–10
cmh
oriz
onan
d20
.32µ
g/g
for
10–4
0cm
hor
izon
wit
hle
ssth
an2%
ofth
eto
tal
Hg
bein
gbi
oava
ilabl
e)
Th
ree
agri
cult
ure
crop
plan
ts:T
riti
cum
aest
ivum
(wh
eat)
—te
rres
tria
lH
orde
umvu
lgar
e(b
arle
y)—
terr
estr
ial
Lupi
nus
lute
us(y
ello
wlu
pin
)—te
rres
tria
l
Th
ede
crea
seof
mea
nH
gco
nce
ntr
atio
nfr
om29
.17µ
gg–
1at
0–10
cmh
oriz
onto
20.3
2µ
gg–
1at
10–4
0cm
hor
izon
dem
onst
rate
dth
ean
thro
pog
enic
orig
inof
the
mer
cury
inth
eso
il.P
relim
inar
yre
sult
ssh
owth
atal
lcro
psex
trac
ted
mer
cury
,wit
hH
gpl
ant
con
cen
trat
ion
reac
hin
gu
pto
0.47
9µ
gg–
1in
wh
eat.
Th
em
ercu
ryco
nce
ntr
atio
nin
the
plan
tsac
cou
nte
dfo
rle
ssth
an3%
ofm
ercu
ryco
nce
ntr
atio
nin
the
soil.
Th
eH
gco
nce
ntr
atio
ns
inth
epl
ants
wer
esi
mila
ror
even
hig
her
than
that
ofth
ebi
oava
ilabl
eH
gin
the
soils
.Mer
cury
extr
acti
onyi
elds
reac
hed
up
to71
9m
g/h
afo
rba
rley
.
-
14 International Journal of Chemical Engineering
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(15)
[56]
Pot
exp
erim
ent
(20
wee
ks)
Soil
from
was
tede
posi
tsof
the
lead
smel
ter
Pb
Agr
osti
sca
pilla
ris—
terr
estr
ial
Inoc
ula
tion
wit
hin
dige
nou
sor
non
indi
gen
ous
AM
Fin
this
expe
rim
ent
did
not
decr
ease
Pb
upt
ake
byth
eh
ost
inco
mpa
riso
nw
ith
non
myc
orrh
izal
plan
tsgr
own
inco
nta
min
ated
soil.
Itca
nbe
con
clu
ded
that
13m
onth
sof
subc
ult
uri
ng
inan
iner
tsu
bstr
ate
did
not
affec
tde
velo
pmen
tof
G.i
ntra
radi
ces
PH
5is
olat
edfr
omth
ew
aste
depo
sits
ofa
Pb
smel
ter
inco
nta
min
ated
soil
ofit
sor
igin
.T
he
inte
ract
ion
ofth
efu
ngu
sw
ith
the
hos
tpl
ant
was
chan
ged:
the
abili
tyof
the
linea
gecu
ltu
red
wit
hou
tH
Mto
supp
ort
plan
tgr
owth
inP
b-co
nta
min
ated
soil
was
decr
ease
d,w
hile
tran
sloc
atio
nof
Pb
from
plan
tro
ots
tosh
oots
incr
ease
d.
(16)
[38]
Fiel
dan
dgr
een
hou
seex
peri
men
ts
Phy
toex
trac
tion
(As-
and
Pb-
con
tam
inat
edso
il)
Ars
enic
(As)
and
lead
(Pb)
Ch
ines
eB
rake
Fern
s(P
teri
svi
ttat
a)—
terr
estr
ial
Indi
anM
ust
ard
(Bra
ssic
aju
ncea
)—te
rres
tria
l
Itap
pea
rsth
atE
DTA
isn
eces
sary
for
Pb
extr
acti
ondu
eto
the
low
soil
Pb
bioa
vaila
bilit
y.So
ilam
endm
ents
like
ED
TAar
en
eces
sary
beca
use
they
mob
ilize
soil
Pb,
mak
ing
itav
aila
ble
topl
ant
root
s.It
may
not
bead
visa
ble
toap
ply
ED
TAin
the
envi
ron
men
t,be
cau
seE
DTA
mob
ilize
sm
etal
s,w
hic
hm
ayle
ach
into
surr
oun
din
gpr
oper
tyof
grou
ndw
ater
.Th
epr
esen
ceof
oth
erm
etal
sth
atco
mpe
tefo
rE
DTA
may
incr
ease
the
amou
nt
ofE
DTA
requ
ired
for
Pb
rem
edia
tion
.
-
International Journal of Chemical Engineering 15
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(17)
[27]
Labo
rato
ryex
peri
men
t,u
sin
gch
ambe
r(6
wee
ks)
Phy
tost
abili
zati
on(m
ercu
ry-c
onta
min
ated
soil
use
din
this
exp
erim
ents
was
obta
ined
from
ach
emic
alfa
ctor
ylo
cate
din
the
sou
thea
stpa
rtof
Pola
nd,
wh
ich
has
been
inop
erat
ion
for
over
50ye
ars)
Hg
Spec
ies
Fest
uca
rubr
a(r
edfe
scu
e)—
terr
estr
ialP
oapr
aten
sis
(mea
dow
gras
s)—
terr
estr
ial
Arm
orac
iala
path
ifol
ia(h
orse
radi
sh)—
terr
estr
ial
Hel
iant
hus
tube
rosu
s(J
eru
sale
msu
nfl
ower
)—te
rres
tria
lS.
vim
inal
is(w
illow
)—te
rres
tria
l
Th
eh
igh
est
con
cen
trat
ion
sof
mer
cury
wer
efo
un
dat
the
root
s,bu
ttr
ansl
ocat
ion
toth
eae
rial
part
also
occu
rred
.Mos
tof
the
plan
tsp
ecie
ste
sted
disp
laye
dgo
odgr
owth
onm
ercu
ryco
nta
min
ated
soil
and
sust
ain
eda
rich
mic
robi
alpo
pula
tion
inth
erh
izos
pher
e.A
nin
vers
eco
rrel
atio
nbe
twee
nth
en
um
ber
ofsu
lfu
ram
ino
acid
deco
mpo
sin
gba
cter
ia,a
nd
root
mer
cury
con
ten
tw
asob
serv
ed.
Th
ese
resu
lts
indi
cate
the
pote
nti
alfo
ru
sin
gso
me
spec
ies
ofpl
ants
totr
eat
mer
cury
-con
tam
inat
edso
ilth
rou
ghst
abili
zati
onra
ther
than
extr
acti
on.
(18)
[57]
Fiel
d(J
uly
and
Oct
ober
)P
hyto
extr
acti
onan
dph
ytos
tabi
lisat
ion
(soi
l)Z
n,C
u,C
ran
dC
d
Two
popl
arcl
ones
(Pop
ulus
delt
oide
sx
max
imow
iczi
i-cl
one
Eri
dan
oan
dP.
xeu
ram
eric
ana-
clon
eI-
214)
—te
rres
tria
l
Leaf
,ste
m,r
oot
and
woo
dycu
ttin
gbi
omas
ses
oftr
eate
dpl
ants
wer
esi
gnifi
can
tly
grea
ter
than
thos
ein
the
con
trol
sin
both
clon
es,e
xcep
tfo
rst
embi
omas
sat
the
begi
nn
ing
ofO
ctob
er.
Am
ong
the
fou
rh
eavy
met
als
(Zn
,Cu
,C
r,an
dC
d),o
nly
Zn
,Cu
,an
dC
rco
nce
ntr
atio
ns
inpl
ants
diff
ered
con
sist
entl
ybe
twee
ncl
ones
orso
iltr
eatm
ents
,wh
ileC
dle
vels
wer
eal
way
sbe
low
the
dete
ctio
nlim
its.
(19)
[58]
Fiel
dst
udy
and
labo
rato
ryex
per
imen
t(2
002-
2003
(fiel
dst
udy
),3
mon
ths
for
labo
rato
ryex
peri
men
t)
Soil
Fe,Z
n,P
b,C
u,N
i,C
r,M
nB
rach
ythe
cium
popu
leum
Th
ere
sult
sob
tain
edfr
omth
isst
udy
onB
.pop
uleu
mle
adto
the
infe
ren
ceth
atph
ysio
logi
cal/
bio-
chem
ical
anal
ysis
ofep
iphy
tic
bryo
phyt
esca
nse
rve
asco
st-e
ffec
tive
indi
cato
rs/m
onit
ors
for
the
envi
ron
men
talq
ual
ity
ofan
yar
ea,a
nd
onth
eba
sis
ofth
isin
form
atio
nap
prop
riat
est
eps
can
beta
ken
toim
prov
eth
eai
rqu
alit
yof
anar
ea.
-
16 International Journal of Chemical Engineering
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(20)
[59]
Pot
expe
rim
ent
and
fiel
dtr
ial(
2004
-200
5fo
rpo
tex
per
imen
t,an
d20
05fi
eld
tria
l)
Phy
toex
trac
tion
and
phyt
osta
biliz
atio
n(s
oil)
As,
Co,
Cu
,Pb,
and
Zn
Th
ree
popl
arsp
ecie
s(P
opul
usal
ba,P
opul
usni
gra,
Popu
lus
trem
ula)
and
Salix
alba
—te
rres
tria
l
Trac
eel
emen
tco
nce
ntr
atio
ns
wer
em
uch
hig
her
inro
ots
than
inab
ove-
grou
nd
tiss
ues
,wit
hpa
rtic
ula
rly
hig
hco
nce
ntr
atio
ns
infi
ne
root
s.T
he
hig
hes
tac
cum
ula
tion
sw
ere
mea
sure
din
P.ni
gra
and
S.al
ba.I
nw
ood,
the
hig
hes
tco
nce
ntr
atio
ns
ofC
uan
dZ
nw
ere
inS.
alba
.Sal
ixal
bafo
liage
con
tain
edh
igh
est
con
cen
trat
ion
sof
As,
Cu
,Pb,
and
Zn
;lea
fZ
nco
nce
ntr
atio
nex
ceed
edth
ose
ofw
ood
byal
mos
t6
tim
es.T
he
over
allr
emov
alof
trac
eel
emen
tsw
ason
lysi
gnifi
can
tly
hig
her
inP.
alba
than
inS.
alba
;P.a
lba.
(21)
[60]
Pot
expe
rim
ent
and
fiel
dtr
ial(
2ye
ars
(200
4-20
05)
for
pot
expe
rim
ent
and
fiel
dtr
ialo
nM
ay–S
epte
mbe
r20
05)
Phy
toex
trac
tion
and
phyt
osta
biliz
atio
n(s
oil
(Pyr
ite
ore
con
tain
sm
ain
lypy
rite
(FeS
2),
less
eram
oun
tsof
chal
copy
rite
(Cu
FeS 2
),sp
hal
erit
e(Z
nS)
,m
agn
etit
e(F
e 3O
4),
and
vari
ous
trac
eel
emen
ts))
As,
Co,
Cu
,Pb
and
Zn
P.al
baL
.(w
hit
epo
plar
)—te
rres
tria
lP.
nigr
aL.
(bla
ckpo
plar
)—te
rres
tria
lP.
trem
ula
L.(E
uro
pea
nas
pen
)—te
rres
tria
lSa
lixal
baL
.(w
hit
ew
illow
)—te
rres
tria
l
Th
ere
sult
show
nth
ates
tabl
ish
men
tof
Popu
lus
and
Salix
spec
ies
atth
esi
teis
ach
ieva
ble
thro
ugh
ripp
ing
ofth
esu
rfac
e,m
inim
alti
llage
,som
em
ixin
gof
the
was
tes
wit
him
port
edso
il,ir
riga
tion
and
fert
ilise
rs.P
oten
tial
ly,t
he
elev
ated
con
cen
trat
ion
sof
Pb,
As
and
oth
erel
emen
tsco
uld
bele
ach
edfr
omth
ere
med
iate
dw
aste
sto
war
dsgr
oun
dwat
eror
oth
erre
cept
ors,
and
thes
efl
uxe
sco
uld
also
bein
flu
ence
dby
soil
amen
dmen
ts,
chan
ges
inth
erh
izos
pher
eor
both
.Im
mob
ilisa
tion
oftr
ace
elem
ents
inbo
thco
arse
and
fin
ero
ots
may
redu
cele
ach
ing,
part
icu
larl
yof
Cu
and
Zn
but
also
As
and
Pb.
-
International Journal of Chemical Engineering 17
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(22)
[61]
Gre
enh
ouse
Phy
toex
trac
tion
and
phyt
osta
biliz
atio
n(s
oil)
Six
sedi
men
t-de
rive
dso
ilsw
ith
incr
easi
ng
fiel
dC
dle
vels
(0.9
–41.
4m
g/kg
)
Two
will
owcl
ones
(Sal
ixfr
agili
s“B
elgi
sch
Roo
d”an
dSa
lixvi
min
alis
“Aag
e”)—
terr
estr
ial
No
grow
thin
hib
itio
nw
asob
serv
edfo
rbo
thcl
ones
for
any
ofth
etr
eatm
ents
.D
ryw
eigh
tro
otbi
omas
san
dto
tals
hoo
tle
ngt
hw
ere
sign
ifica
ntl
ylo
wer
for
S.vi
min
alis
com
pare
dto
S.fr
agili
sfo
ral
ltr
eatm
ents
.Will
owfo
liar
Cd
con
cen
trat
ion
sw
ere
stro
ngl
yco
rrel
ated
wit
hso
ilan
dso
ilw
ater
Cd
con
cen
trat
ion
s.B
oth
clon
esex
hib
ited
hig
hac
cum
ula
tion
leve
lsof
Cd
and
Zn
inab
ove
grou
nd
plan
tpa
rts.
Cu
,Cr,
Pb,
Fe,
Mn
,an
dN
iwer
efo
un
dm
ain
lyin
the
root
s.B
ioco
nce
ntr
atio
nfa
ctor
sof
Cd
and
Zn
inth
ele
aves
wer
eth
eh
igh
est
for
the
trea
tmen
tsw
ith
the
low
est
soil
Cd
and
Zn
con
cen
trat
ion
.
(23)
[62]
Labo
rato
ryan
dfi
eld
Rh
izob
oxex
peri
men
tw
asu
sed
toin
vest
igat
eth
esh
ort-
term
effec
tof
will
owro
ots
onm
etal
avai
labi
lity
inox
ican
dan
oxic
sedi
men
t.Lo
nge
r-te
rmeff
ects
wer
eas
sess
edin
afi
eld
tria
l(s
oil)
Cd,
Zn
,Cu
,an
dP
bW
illow
(Sal
ixsp
p.)—
terr
estr
ial
Th
erh
izob
oxtr
ials
how
edth
atC
d,Z
n,
and
Cu
extr
acta
bilit
yin
the
rhiz
osph
ere
incr
ease
dw
hile
the
oppo
site
was
obse
rved
for
Pb.
Th
efi
eld
tria
lsh
owed
that
Cu
and
Pb,
but
not
Cd,
wer
em
ore
avai
labl
ein
the
root
zon
eaf
ter
wat
eran
dam
mon
ium
acet
ate
(pH
7)ex
trac
tion
com
pare
dw
ith
the
bulk
sedi
men
t.Se
dim
ent
inth
ero
otzo
ne
was
bett
erst
ruct
ure
dan
dag
greg
ated
and
thu
sm
ore
per
mea
ble
for
dow
nwar
dw
ater
flow
s,ca
usi
ng
leac
hin
gof
afr
acti
onof
the
met
als
and
sign
ifica
ntl
ylo
wer
tota
lco
nte
nts
ofC
d,C
u,a
nd
Pb.
-
18 International Journal of Chemical Engineering
Ta
ble
2:C
onti
nu
ed.
No.
Res
earc
her
Res
earc
hsc
ale
and
dura
tion
Upt
ake
mec
han
ism
san
dm
edia
(su
bstr
ate)
Con
tam
inan
tor
para
met
eran
dco
nce
ntr
atio
nP
lan
tsn
ame
and
typ
eR
esu
lt
(24)
[63]
Pot
expe
rim
ent
Phy
toex
trac
tion
(soi
l)
As
(as
Na 2
HA
sO4),
Cd
(as
CdC
l 2),
Pb
(as
Pb(
CH
3C
OO
) 2),
and
Zn
(as
Zn
(CH
3C
OO
) 2)
(100
mg
As/
kg,4
0m
gC
d/kg
,200
0m
gP
b/kg
,an
d20
00m
gZ
n/k
g)
Salix
spp.
—te
rres
tria
l
Alt
hou
ghA
san
dC
du
ptak
esl
igh
tly
incr
ease
din
Such
dol-
Zn
soil
com
pare
dto
Such
dol-
Pb
soil,
the
elem
ent
rem
oval
from
soil
was
sign
ifica
ntl
yh
igh
erin
Such
dol-
Pb
soil
due
toa
sign
ifica
nt
redu
ctio
nof
abov
egro
un
dbi
omas
syi
eld
inSu
chdo
l-Z
nso
il.T
he
yiel
dre
duct
ion
decr
ease
dth
eu
ptak
eof
plan
t-av
aila
ble
elem
ents
bybi
omas
s;th
us
hig
her
plan
t-av
aila
ble
port
ion
sof
As
and
Cd
wer
efo
un
din
Such
dol-
Zn
soil.
(25)
[64]
Fiel
dsu
rvey
:fro
m12
As-
con
tam
inat
edsi
tes
(Sep
tem
ber
toN
ovem
ber
2003
)
Fiel
dst
udy
:co
nta
min
ated
soil
As
Sam
ples
of24
fern
spec
ies
belo
ngi
ng
to16
gen
era
and
11fa
mili
esas
wel
las
thei
ras
soci
ated
soils
wer
eco
llect
ed—
terr
estr
ial
Pte
ris
mul