Phytofiltration of Heavy Metals

6.18 Phytofiltration of Heavy Metals: Assessment of the Key Factors Involved in the Design of a Sustainable Process EJ Olguín and G Sánchez-Galván, Institute of Ecology, Xalapa, México © 2011 Elsevier B.V. All rights reserved.

6.18.1 Introduction 6.18.2 Selection of the Plant Species Offering the Best Performance 6.18.3 Selection of the Most Appropriate Phytofiltration System 6.18.4 Factors Affecting Metal Uptake by Plants 6.18.5 Treatment and Disposal of Biomass Containing Metals 6.18.6 Concluding Remarks References Relevant Websites

Glossary constructed wetlands Engineered systems that have been designed to treat wastewaters, in a more controlled environment, taking advantage of many of the processes that occur in natural wetlands. lagoons Shallow ponds in which plants float on the surface. macrophytes Aquatic plants growing in or near water that are emergent, submergent, or floating.

207 207 209 209 210 212 212 213

phytochelatins Peptides that bind heavy metals; they are enzymatically synthesized in plant cells. phytofiltration Use of plants and their associated rhizospheric microorganisms to remove contaminants from water and aqueous waste streams. pyrolysis Thermochemical decomposition of organic material occurring in the absence of oxygen.

6.18.1 Introduction Heavy metals are pollutants of inorganic origin that contaminate surface water and groundwater as a consequence of natural events and human activities. Their release into the environment presents a serious threat due to their cytotoxic, mutagenic, and carcinogenic effects on human beings and wildlife [1]. Different technologies such as chemical precipitation, coagulation– flocculation, flotation, ion exchange, and membrane filtration have been developed to remove heavy metals from contaminated wastewaters. However, they have inherent limitations mainly due to the lack of economical feasibility for the treatment of large volumes of water with a low metal concentration. The biological treatment of metals, especially phytoremediation, is becoming a more attractive alternative. It is an emergent field in which active research is performed around the world. Phytofiltration, a specific strategy of phytoremediation, is the use of plants to remove contaminants from water and aqueous waste streams [2]. Three different phytofiltration systems have been described: (1) rhizofiltration (the use of hydroponically cultivated plant roots); (2) constructed wetlands (CWs) and lagoons; and (3) bioadsorbent-based systems [1]. Due to space limitations, only aspects related to CWs and lagoons will be discussed herewith. The different factors that influence the performance of such systems have been described, including composition of the supporting media and sediment, pH, and type of wastewater. However, there are other key factors that have to be taken into account for the design of a phytofiltration system. One of the common questions made by possible users of the phytofiltration technologies is the availability of methods for the final use and disposal of the contaminated plant biomass. However, there is scanty information dealing with this particular issue and further research is required. Thus, the aim of this article is to present a discussion of the main factors affecting the design of sustainable processes for phytofiltration of heavy metals, such as the selection of the plant species, especially from tropical and subtropical regions, the selection of the appropriate phytofiltration system, the environmental conditions affecting metal uptake by plants, and the treatment and disposal of biomass containing metals, and whenever possible, the recovery of metals at the end of the process.

6.18.2 Selection of the Plant Species Offering the Best Performance For some decades, research has been performed mainly with plants commonly occurring in temperate and cold climates and it is only in the recent years that more research has been carried out with tropical plants. There is a need for searching for new plants, taking advantage of the large biodiversity found in subtropical and tropical regions of the planet. The following discussion has

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been limited to floating macrophytes, since they constitute a major component of freshwater environments in terms of biodiversity, ecosystem functions, biomass, and species richness [3]. Additionally, floating macrophytes have been shown to be very efficient in the removal of heavy metals from water and wastewaters. Low-cost production, abundance in aquatic ecosystems, and easy handling are some of their advantages. A variety of polluted waters can be phytoremediated, including sewage and municipal wastewater, agricultural runoff/drainage water, industrial wastewater, coal pile runoff, landfill leachate, mine drainage, and groundwater plumes [1]. Phytotechnologies using macrophytes and applied in tropical and subtropical environments have advantages such as longer plant-growing seasons and increased temperature, which can accelerate the contaminant removal processes. Different metal accumulation capacities have been found, which also depend on various factors such as metal concentration in the effluent, kind of effluent, pH, temperature, irradiance, the presence of nutrients, and the presence of other metals. Thus, the metal concentrations recently reported in macrophytes can be classified within three ranges (Table 1): (1) high (10 000–100 000 mg kg−1) (2) medium (1000–9999 mg kg−1) and (3) low (100–999 mg kg−1). High metal concentrations have been obtained within free-floating plants such as Salvinia minima [4, 5]. Very high lead concentrations (100 000 mg kg−1) have been found in this aquatic fern during the metal removal process in continuous-operated lagoons, which were attributed not only to the effect of environmental conditions (such as high temperature and irradiance), but also to the unique characteristics of this aquatic plant [6]. The surface of S. minima has extraordinary physicochemical characteristics such as a high specific surface (264 m² g−1) and an important content of carboxyl groups (0.95 mmol H+ g−1 dw), which are excellent properties for metal sorption. Thus, it has been demonstrated, over a wide range of Pb2+ concentrations (0.8–28 mg l−1), that the main lead uptake mechanism occurring in this plant is biosorption, whereas intracellular accumulation plays a secondary role [7]. On the contrary, in the case of Hydrilla verticillata, a significant proportion of Zn was accumulated intracellularly (70%) while the rest was adsorbed on the surface in a range of Zn2+ concentrations of 100–5000 μM [8]. The concentration of lead in the plant tissue is determined not only by the intrinsic properties of the plant species but also by environmental factors i.e., the concentration of the metal in the solution as mentioned before, and the type of exposure system utilized. The concentration found in S. minima in batch systems was nearly half of that found in continuous systems for the same initial concentration of metal (Table 1). Eichhornia crassipes is a very well-known macrophyte and has been the subject of extensive research on phytofiltration, due to its high growth rate and well-known aggressiveness to become a dominant species and a weed in polluted freshwater reservoirs. Recently, it has been considered as an efficient and reliable Cd2+ accumulator since it does not release the absorbed Cd back to the environment but stores the metal in its tissues in the form of a stable high-molecular-weight complex characterized as a phytochelatin (PC) [9]. In other studies also performed with E. crassipes [10], it was found that 99.8% of the lead uptaken remained in the roots with no translocation to the leaves, indicating that once the plant is harvested, roots could be treated for recovery of metals and leaves could be reused for composting or other techniques. Furthermore, it was observed that the highest Pb2+ concentration in the tissue was observed at the highest concentration tested (Table 1), confirming the influence of the concentration of the metal in solution upon the removal process. It is also known that the submerged floating rootless macrophyte, Ceratophyllum demersum, accumulates various heavy metals. Mishra et al. [11] found that plants accumulate high amounts of Pb2+ and the production of PCs seems to be the potential detoxification mechanism, indicating that this plant appears to have the potential for its use as a phytoremediator species in aquatic environments. Compared to other macrophytes (Table 1), low metal concentrations have been observed in duckweeds. It has been reported that Lemna minor is able to accumulate Pb2+, and Ni2+ from a coal mine effluent mainly in the roots. Maximum removal of such Table 1

Metal concentration in the tissue of various floating macrophytes Metal concentration

Scientific name

Water column (mg l−1) 2+

Salvinia minima

Pb

28

Eichhornia crassipes

Pb2+

Hydrilla verticillata Eichhornia crassipes

Zn2+ Pb2+ Cd2+ Pb2+ Hg2+ Pb2+ Ni2+

200 100 327 15 1.12 20.74 3 0.15 0.49

Ceratophyllum demersum Azolla pinnata Lemna minor

a

Continuous systems. Batch systems. c Real effluents containing various metals. b

Biomass (mg kg−1dw) 100 000 50 600b 36 670 18 653 18 070 4 865 3 000 1 748 667 180.70c 114.50c

a

Reference [6] [7] [10] [10] [8] [10] [9] [11] [13] [11] [12]

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metals was observed when the system was operated at a hydraulic retention time (HRT) of 20 days [12]. Azolla pinnata has been shown to uptake Hg2+ from aqueous solutions. The metal concentration in the tissue was directly related to that of the solution, although the plant growth was inhibited up to 27.0–33.9% in the presence of the heavy metal [13].

6.18.3 Selection of the Most Appropriate Phytofiltration System CWs are engineered systems that have been designed to treat wastewaters, in a more controlled environment, taking advantage of many of the processes that occur in natural wetlands [14]. The plants and their associated microbes remove and recycle metals from either the water or sediments. The sediments, biotic components (plants and microorganisms), and detritus (dead organic matter) are the major storage components [15]. They are a cost-effective and technically feasible technology. The expenses of operation and maintenance (energy and supplies) are low, requiring only periodic, rather than continuous, on-site labor. Furthermore, CWs are tolerant to fluctuations in flow and facilitate water reuse and recycling [2]. The basic classification of CWs is based on the type of flow regime and macrophytic growth. In general terms, two types can be described: (1) the surface flow CWs (SFCWs) and (2) the subsurface flow CWs (SSFCWs). SFCWs are shallow sealed basins or a sequence of basins, containing 20–30 cm of rooting soil, with a water control structure that maintains a shallow depth of water (less than 0.4 m). The water surface above the soil is aerobic, while the deeper waters and substrate are usually anaerobic. Dense emergent vegetation covers usually more than 50% of the surface. However, leave-floated, submerged, and floating macrophytes are also found [15]. Their capital and operating costs are low. However, their main disadvantage is that a larger land area is required than other systems. On the other hand, SSFCWs are gravel and/or soil/sand-filled trenches, channels, or basins with no standing water, which support emergent vegetation. Two types of SSFCWs have been described: the horizontal-flow SSFCWs (HFCWs) and the verticalflow CWs (VFCWs). In the former, the wastewater flows slowly through the bed in a relative horizontal path and comes into contact with a network of aerobic, anoxic, and anaerobic zones. Finally, VFCWs are fed intermittently to flood the surface and wastewater, then gradually percolate down through the bed and is collected by a drainage network at the base [16]. SSFCWs have some advantages over SFCWs: (1) a greater cold tolerance; (2) minimization of pests, such as mosquito larvae, and odor problems; and (3) a greater assimilation potential per unit of land area, which results in a smaller requirement of land for the same volume of wastewater. On the other hand, SSFCWs are more expensive to construct and may be more difficult to regulate than SFCWs. Furthermore, maintenance and repair costs are generally higher. Clogging and unintended surface flow problems have also been reported for this kind of system. Lagoons with free-floating macrophytes consist of one or more shallow ponds in which plants float on the surface. They are shallow enough to ensure adequate contact between the roots of the floating plants and the wastewater (depth range: 0.9–1.5 m) [2]. These systems are an effective and reliable water reclamation technology if they are properly designed, constructed, operated, and maintained. They have proved to be effective in removing metals from municipal and industrial wastewaters and stormwater [1]. The selection of the most appropriate option should be according to various operational factors and the plants available in the region where the phytofiltration system is expected to operate [1]. Regarding the economical assessment, some key factors must be considered such as (1) construction costs, (2) equipment and labor costs, (3) value of land used for the system, and (4) cost of operation and maintenance. In the case of ponds with floating plants, the number, size, and arrangement of ponds and the method of harvesting must be taken into account.

6.18.4 Factors Affecting Metal Uptake by Plants Factors affecting metal uptake and distribution within living plants include (1) physical and chemical properties of the metal (e.g., water solubility and molecular weight), (2) plant characteristics (e.g., surface characteristics, root system, and type of enzymes), and (3) environmental characteristics [17] (Figure 1). Only environmental factors are discussed in this section, due to space limitations. Environmental factors are physicochemical conditions that alter metal uptake. Thus, a higher Zn2+, Cu2+, and Cd2+ uptake has been observed when temperature was increased from 5 to 20 °C in systems with Potamogeton natans [18]. The effect of light intensity and temperature on the Pb2+ uptake capability of S. minima in continuous systems was assessed [6]. It was found that there was an optimal range for both parameters (650 μmol m−2 s−1 and 25.33 °C) and that an extremely high concentration of Pb2+ (87 000mg kg−1) was observed under these conditions. However, it has also been observed that a very high temperature diminished metal uptake. Uysal and Taner [19] found a peak in Pb2+ concentration in L. minor tissue when temperature increased up to 30 °C (8622 mg kg−1). Subsequently, it decreased as temperature increased up to 35 °C (3021 mg kg−1). On the other hand, the effect of pH on metal speciation and uptake has been widely discussed. Lower pH generally increases metal uptake mainly because the solubility of many metals increases as the pH decreases within a certain range. For example, Pb2+ uptake by L. minor decreased at pH 4.5–6.0 range, but it did not change above pH 6.0 [19]. On the contrary, the water lily Nymphaea aurora absorbed more Cd2+ at a pH of 5.5 (140 mg g−1) than at a pH of 4.0 (60 mg g−1) [20]. It is known that salt (NaCl) treatment reduces the activity of the free Cd2+ in solution due to competition, resulting in the alleviation of metal toxicity. However, the mechanism has not yet been elucidated. In this context, and designing an experiment that

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pH Cations

Temperature

Anions

Metal uptake

Organic matter

Irradiance

Other metals Salinity

Figure 1 Environmental factors affecting metal uptake in plants in aquatic systems.

had the same Cd2+ activity, Xu et al. [21] found that mild concentrations of NaCl alleviated the toxicity of Cd2+ on the growth of Arabidopsis thaliana and Solanum nigrum cultivated hydroponically. As a consequence, a higher production of proline, glutathione, and PCs (detoxification mechanisms) was observed. At the same time, the Cd2+ uptake, in the roots (64.3%) and in the shoots (83.7%) of S. nigrum, was increased. On the contrary, the supply of salinity reduced the Cd2+, Cu2+, and Zn2+ concentrations in tissues of Elodea canadensis and P. natans, but unlike the other metals, Pb2+ accumulation was unaffected or very less affected by salinity [18]. The presence of organic matter and sediments is a key factor in metal removal, especially in CWs. It is known that the surface component of the wetland favors sedimentation and binding of metals to the organic matter on the top of the sediment, which tends to be anoxic with reducing conditions, acting as a sink for metals [22]. In fact, filtration and chemical precipitation through contact of the water with the substrate and litter, and adsorption and ion exchange on the surfaces of substrate, sediment, and litter are two of the main mechanisms of metal removal in CWs [1]. However, in a hydroponic culture of Lolium perenne, humic acid reduced Cu2+, Pb2+, and Fe2+ adsorption at the root surface, but it increased the adsorption of Cd2+, Zn2+, and Mn2+ at the same surface [23]. It is known that anions and cations can increase or reduce metal uptake in plants, especially in systems with macrophytes. Olguín et al. [5] concluded that the fate of Pb2+ in batch-operated lagoons with S. minima, including plant accumulation, was primarily a function of the presence of certain nutrients or ligands, such as Ethylenediaminetetraacetic acid (EDTA) and phosphates. Lead forms soluble and insoluble complexes with such nutrients, thereby inhibiting metal uptake by plants. On the contrary, the presence of other cations and anions such as magnesium, sulfate, and propionate did not reduce Pb uptake in this aquatic fern [7], as previously described for other systems [17]. Finally, the presence of other metals can have antagonistic (nonadditive) or synergistic effects on metal uptake/toxicity. It is known that the presence of Zn2+ is antagonistic with respect to Cd2+ uptake [17]. On the other hand, a synergistic relationship between Fe2+ uptake and Cd2+ has been demonstrated in Phragmites australis [24]. Furthermore, a higher positive relationship was observed in the presence of Cu2+ than regarding the presence of Cd2+ for Fe2+/Fe3+ uptake in Matricaria chamomilla cultivated hydroponically [25].

6.18.5 Treatment and Disposal of Biomass Containing Metals Handling and disposal of metal-contaminated biomass is one of the main concerns while designing a sustainable heavy metal phytofiltration process. It has been described that senescent plant tissues may be sources of metal release through leaching or can be sinks for metals through litter adsorption or microbial immobilization. The residence time of metals in plants and systems can be affected by the extent of uptake and how metals are distributed within biomass [17]. Thus, different methods have been proposed for the treatment of biomass contaminated with metals (Figure 2). Composting, compaction, and pyrolysis are considered pretreatments, since a significant amount of contaminated biomass will remain thereafter. The methods for final disposal (or posttreatments) include direct disposal, liquid extraction, and co-firing with coal [26]. Finally, different energy recovery techniques have also been proposed to convert metal-contaminated biomass into bioenergy [27]. Composting has been proposed as a pretreatment step before disposal of metal-rich biomass, especially after being used in a phytoextraction process, but it could also be employed for biomass produced after a phytofiltration process. However, drying of the biomass before composting might be necessary, since anaerobic conditions may arise due to an excess of water. Composting has

Phytofiltration of Heavy Metals: Assessment of the Key Factors Involved in the Design of a Sustainable Process

Pretreatments

Posttreatments

Bioenergy production

Composting

Direct disposal

Gasification

Synthetic gas

Compaction

Liquid extraction

Incineration

Heat

Pyrolysis

Co-firing with coal

Anaerobic digestion

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Biogas + fertilizer

Figure 2 Methods for metal extraction from contaminated biomass after phytofiltration.

shown to be effective for treating arsenic-rich biomass (Pteris vittata) before disposal in a landfill [26]. Biomass was reduced by 38% and As by 25–32%, whereas the contaminant had just a little detrimental effect on microorganisms involved in the composting process. Nevertheless, As3+ was removed mainly through the compost leachate, which required to be collected for a safe disposal. Volatilization and immobilization of arsenic were secondary mechanisms of As loss. On the other hand, the objective of pyrolysis is to concentrate heavy metals in the ash/char fraction after thermal treatment, preventing them from being released in the condensable and/or volatile fractions. Some of the key parameters in this process in terms of maximum recovery are the temperature and the type of solid heat carrier (e.g., sand and fumed silica) [28]. Liquid extraction is one of the most widely reported posttreatment steps for metal recovery. It is commonly carried out through chemical leaching, in which detoxified biomass is converted to a suitable fertilizer or mulch. Recovery of more than 97% of Ni2+ was obtained from seeds of the hyperaccumulator Alyssum murale using H2SO4 solution at 90 °C with a 15% solid concentration during 120 min. The use of a three-step countercurrent extraction process removed the Ni2+ almost completely (99.0%) from the seeds [29]. Additionally, ammonia–ammonium chloride solution has also been used successfully as a leaching agent for recovery of Zn2+ from Sedum plumbizincicola biomass. The results indicated that leaching temperature had the most dominant effect on metal extraction performance, followed by nNH4Cl/nNH3 ratio, solid/liquid ratio, and leaching time. The total zinc removal after leaching under the optimum conditions reached 97.95%. The thermodynamic study indicated that the dominant species produced by the leaching process was the soluble species Zn(NH3)42+ [30]. There are only a few reports related to the use of chemical leaching for metal recovery from aquatic plants. Nuñez et al. [31] evaluated the leaching of lead from S. minima biomass using several aqueous ammonium salts and EDTA solution as Pb extractants. EDTA was the most efficient leachant, followed by ammonium oxalate, with ammonium acetate being very inefficient (99%, 70%, and 1.3% recovery, respectively). According to the thermodynamic study, the dominant species produced by the leaching process is the soluble species PbEDTA2– for the EDTA system and the insoluble Pb(COO)2S precipitate for the oxalate system. Thus, the authors concluded that the use of ammonium oxalate for the recovery of Pb2+ from the leachate was more convenient compared to the use of EDTA, even though both were efficient leachants. Furthermore, the biomass became enriched in ammonium and could still be used as a fertilizer, after the recovery of metals. A similar procedure was also successfully applied for the treatment of E. crassipes biomass contaminated with lead [10]. Another posttreatment process is co-firing, which is a low-cost option for converting biomass, efficiently and cleanly, to electricity by adding biomass as a partial substitute fuel in high-efficiency coal boilers. In addition to the reduction of CO2 emissions, this treatment also contributes to the decrease of sulfurous gas emissions (i.e., sulfur dioxide) and therefore to the reduction of acid rain, since the biomass contains significantly less sulfur than most coal. Co-firing was found to reduce the leadcontaminated mass by nominally 90% by concentrating the lead into the smaller fly ash particles [32]. Finally, there are methods that have a dual purpose, metal recovery and energy generation in the form of heat, synthetic gas, biogas, and so on. Gasification and incineration, being thermal treatments, have been described as feasible options for separating metals from the plant residues. Keller et al. [33] used a lab-scale reactor to simulate the volatilization behavior of heavy metals in a grate furnace. The results showed that gasification (reducing conditions) was a better method than incineration (oxidizing conditions) to increase volatilization and hence subsequent recovery of cadmium and zinc from Thlaspi caerulescens and Salix viminalis biomass. It would also allow recycling of the bottom ash as a fertilizer. Biogas production from biomass contaminated with metals has been tested with water hyacinth (E. crassipes) and water chestnut (Trapa bispinosa) employed for phytoremediation of toxic metal effluents. Maximum cumulative production of biogas was 2430 cc ml per 100 g dw−1 of water hyacinth and 1940 cc ml per 100 g dw−1 of water chestnut, and methane content was 63.82% for water hyacinth and 57.04% for water chestnut. The qualitative and quantitative variations in biogas production were correlated with the chemical oxygen demand (COD), carbon, nitrogen, carbon/nitrogen (C/N) ratio, and toxic metal contents of the slurry used [34].

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6.18.6 Concluding Remarks The design of a sustainable phytofiltration process for the removal of heavy metals should take into account a sequence of decisions and the knowledge already available. The first step is to select the plant species that is most suitable for the geographical region in which the system is expected to operate. Tropical and subtropical regions offer a great biodiversity, and this needs to be explored in depth for selecting plants with intrinsic and unique characteristics favoring metal uptake. Within the floating macrophytes, there are some very promising species that have shown to be able to accumulate very high metal concentration in their biomass, especially in continuous systems. Thus, a lot more studies using this type of system should be performed. The second important decision is related to the selection of the most appropriate phytofiltration system. The cost of construction and operation is an important factor, and also the land availability and the easiness of operation. Each type of system has its own advantages and disadvantages, and the challenge is to choose the one that offers the best performing characteristics for a particular situation. It is essential to know the effect of most of the environmental factors on each particular system, so that proper adjustment of parameters can be done. Once the selection of the plant species and the phytofiltration systems has been performed, the adjustment of particular operational conditions may help to achieve the highest removal percentages for a particular metal or a mixture of them. Also, studies of compartmentalization of the metal within the plant may allow predicting whether the roots should be properly disposed and a further use of the leaves could be envisaged, in case where no translocation of metals had been observed. Harvesting frequency is also an essential parameter that should be established for each system. Finally, a very important issue that demands a lot more of research and evaluation on a large scale is the one related to the posttreatment of the contaminated plant biomass. To involve such unit operation ensures the sustainability of the whole process. There is scanty information about the technical and economical feasibility of some of the few processes that have been proposed. The chemical leaching of the biomass with salts such as ammonium oxalate seems to be very promising, since the treated biomass that results is free of metals and ammonium-enriched, facilitating not only proper disposal of the biomass but also production of a new coproduct (fertilizer). Recovery of certain metals with high market value is also an area of opportunity. In the context of the current need for developing alternative fuels to the fossil fuels, the production of biogas from the treated biomass also seems to offer an opportunity niche.

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Relevant Websites http://www.nrel.gov/ – National Renewable Energy Laboratory. http://www.epa.gov/ – United States Environmental Protection Agency. http://www.wsi.nrcs.usa.gov/–