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One step forward, two steps back: the evolution of phytoremediation into commercial technologies

One step forward, two steps back: the evolution of phytoremediation into commercial technologies BioscienceHorizons Volume 7 2014 10.1093/biohorizons/hzu009 Review One step forward, two steps back: the evolution of phytoremediation into commercial technologies Chloe Stephenson* and Colin R. Black School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK *Corresponding author: Tel: +44 07909912125. Email: stepcj@hotmail.co.uk Supervisor: Colin R. Black, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK. Tel: +44 01159516337. Email: colin.black@nottingham.ac.uk This review charts the evolution of phytoremediation from its earliest beginnings, with the discovery of metal tolerant plants in the 16th century and metabolism of organic pollutants by plants in the 1940s. The rapid expansion of research in the early 1990s led to many crucial discoveries but failed to surmount the fundamental limitations that often impede commercial appli- cation of phytoremediation. It is argued that phytoremediation was saved from being forgotten by its evolution under the new term phytotechnology, or ‘the application of science and engineering to examine problems and provide solutions using plants’. This review explores the use of phytotechnology for ecological engineering using constructed wetlands and evapo- transpiration caps as landfill covers. Finally, the transfer of phytotechnology to developing countries, where it has great potential to solve the growing problem of pollution, is examined. The development of phytotechnology can be perceived as an illustration of the modern evolution of scientific thought, from the traditional reductionist view to a wider holistic approach which takes into account the natural environment and our need to preserve it. It is hoped that the evolution of both will allow for increasing conservation of finite resources without sacrificing continued development. Key words: phytoextraction, phytoremediation, phytomining, phytotechnologies, structured wetlands, infiltration caps Submitted on 6 January 2014; accepted on 21 August 2014 Introduction Disposal of industrial waste was previously regarded as a non-productive function to be achieved at least possible cost The Oxford Dictionary (2013) defines a paradigmatic shift as (Hamlin, 2002). In the race for progress and prosperity, this led ‘a fundamental change in approach or underlying assump- to extensive pollution, causing the Global Assessment of Soil tions’. Such shifts occur as evidence accumulates to dispute Degradation to estimate that 21.8 × 10 ha of land in Europe, old ideas and support new ones (Kuhn, 2012), and may argu- Asia, Africa and Central America was affected by chemical pol- ably have occurred in the way humanity views the natural lutants (Alloway, 2001). Chemical pollution of soil may involve environment; a widely cited origin for such a shift is Rachel both inorganic and organic compounds. The former include Carson’s (1962) book, ‘A Silent Spring’, which recognized trace metals, which occur naturally in all soils, but whose con- the complex and vital role of soil in regulating the biosphere, centration may increase following release from diverse anthro- ‘the thin layer of soil that forms a patchy covering over the pogenic sources including metalliferous mining, smelting and continents [which] controls our own existence and that of waste disposal (Alloway, 2001). Two important categories of every other animal of the land’. This was soon followed by pollutants containing organic hydrocarbons include a range of the development of the Gaia principle, which proposed that saturated alkenes and organic components containing nitrogen, living organisms interact with their abiotic environment to sulphur and aromatic hydrocarbons from petroleum and persis- establish complex systems that contribute to maintenance of tent organic pollutants, which are arbitrarily classified as life on Earth (Lovelock, 1967, 2000). ‘organic compounds that are resistant to environmental © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Review Bioscience Horizons • Volume 7 2014 degradation through chemical, biological and photolytic pro- discovered in the 16th Century by Andrea Cesalpino (Brooks, cesses’ (Stockholm Convention, 2008). The definition has been 1998). Realization of the implications of these observations extended to include polycyclic aromatic hydrocarbons and poly- was slow until in 1940 Miller showed that the metabolism of chlorinated biphenyls among others (Alloway, 2001). xenobiotics infused into intact plants was analogous to their transformation and conjugation in mammals (Sandermann, Recognition of the threat posed by pollution in the USA 1994). Margazzi and Vergano (1948) reported the accumula- forced changes in legislation (Hamlin, 2002). The 1965 tion of nickel (Ni) in Alyssum bertolonnii to concentrations of Waste Disposal Act was the first to regulate waste on a upto 0.79% from soil containing 0.42% Ni (Brooks, 1998). national scale and was followed by the creation of the Environmental Protection Agency (EPA) by President Nixon However, ignorance of these findings led to the view that in 1970. The fines and penalties imposed transformed waste phytoremediation was impossible as it was assumed that high disposal from a non-productive function to a productive ven- soil metal concentrations induced matrix toxicity (McCutcheon ture and initiated the search for efficient, cost-effective reme - and Schnoor, 2003), and that plants could not metabolize non- diation technologies for cleaning contaminated sites. Various polar xenobiotics such as the organochlorine insecticide, technologies were developed that focused on stabilization dichlorodiphenyltrichloroethane (DDT; Russell, 2005); these (permeable reactive barriers) or removal (excavation and views were subsequently discredited for both organic and inor- landfill) of pollutants; their primary disadvantage was that ganic compounds. The feasibility of degrading organics was they were clumsy, costly and inefficient ( Hamlin, 2002). elucidated in the ‘green liver model’ of organic metabolism by plants (Sandermann, 1994) and proved by studies of An emerging alternative is phytoremediation, ‘the use of Petroselinium hortense which demonstrated its ability to green plant-based systems to remediate contaminated soils, degrade DDT (Russell, 2005). For inorganic pollutants, the sediments and water’ (Kruger, Todd and Joel, 1997). metal-tolerant species first observed by Andrea Cesalpino were Phytoremediation has the advantage that it may remediate rediscovered by Brooks et al. (1977) who coined the term, soils similarly to traditional techniques, removing or stabiliz- hyperaccumulator, to describe plants able to accumulate 0.1% ing contaminants but, as it relies on plant physiological pro- Ni in dry matter, 100 times greater than the concentrations cesses, is solar-driven and so is typically 10-fold cheaper tolerated by non-accumulator plants (Brooks, 1998), solving (Pilon-Smits, 2005). Another advantage is that phytoremedi- the problem of matrix toxicity. ation is carried out in situ, contributing to its relatively low cost and limiting human and environmental exposure to pol- These discoveries led to realization of the potential of phy- lutants; phytoremediation is popular, because it is perceived toremediation, and rapid advances were made in the early as a clean green technology. This review examines the evolu- 1990s, cemented by the filing of a Japanese patent by tion of phytoremediation of industrial pollutants into a Utsunomiya for the use of plants to extract Cd (McCutcheon widely applicable and commercial technology and reveals its and Rock, 2001). untapped potential for use in developing tropical countries. One step back One step forward Differing research approaches led to a varied uptake of com- mercial phytoremediation in its two largest markets, Europe Although phytoremediation is often described as a ‘new’ and America. In America, funding by organizations such as the technology, this is incorrect as it has arguably evolved over Environmental Protection Agency (EPA) and the Department the past 300 years due to developments in land reclamation, of Defence encouraged application-based research, focusing land farming of oily wastes and improved herbicide, pesticide on real-life contamination scenarios. This resulted in the rela- and agronomic technologies (McCutcheon and Rock, 2001). tive success of commercial phytoremediation, as entrepreneur- During this progression, the fundamental principle of using ial businesses attached to research institutes quickly sprang up. plants for environmental remediation has remained constant, An example of such a company is illustrated later in this arti- but changing paradigms of technology and understanding cle, in Ecolotree’s use of trees on landfill sites ( Ecolotree, 2013). have been superimposed. In contrast, European schemes focusing on fundamental Phytoextraction of trace metals initially received far greater research such as the COST Action 837 have resulted in the attention than organic compounds due to the difficulty of limited success of commercial phytoremediation projects analysing the latter and their transformations (Watanabe, (Schwitzguébel et al., 2002). 1997). However, the origin of both technologies was similar, stemming from early observations of unusual interactions The widely cited report by Glass (1999) captured the prevail- between plants and their environment; for organics, this orig- ing optimism regarding commercialization of phytoremediation inated from observations that concentrations of these pollut- in the USA by reporting that the potential global market for this −1 ants decreased more rapidly in vegetated soils (Salt, Smith and technology had increased from $15–18 bn yr in 1998 to $34– −1 Raskin, 1998). For inorganics, distinctive plant communities 54 bn yr in 1999, predicting that the US market would reach known as serpentine vegetation were identified growing on $235–400 million by 2005. However, the review by Pilon-Smits ultramafic soils with a high Mg and Fe content, as first (2005) included a personal communication from Glass stating 2 Bioscience Horizons • Volume 7 2014 Review that the US phytoremediation market was worth $100–150 mil- traditional breeding techniques to improve plants for lion at that time, and Conesa et al. (2012) observed that ‘virtu- phytoremediaton, particularly for complete degradation of ally none of this potential materialized in the subsequent decade’. organic pollutants by plants (Van Aken, 2008), it soon became This suggests that phytoremediation has not achieved its pre- clear that biotechnology would have a major role in elucidating dicted potential as a commercial technology. biological mechanisms and providing novel genetic material. The first papers detailing the use of transgenics in phytoreme - Phytoremediation is arguably trapped in a vicious cycle diation involved the introduction of a human metallothionein where uncertainty, an affliction of all innovative new tech - into Nicotiana tobaccum L. (tobacco) to increase Cd accumula- nologies (Glass, 1999), discourages the funding required to tion and rabbit esterase in Solanum lycopersicum L. (tomato) finance further research. With the result that phytoremedia - to provide resistance to the herbicide, thiazopyr (Maestri and tion’s limitations remain unsolved. Marmiroli, 2011; Fig. 1). During its development, phytoremediation encountered To solve the problem of bioavailability, the use of soil several fundamental physical limitations of plants which amendments, including chelates such as ethylenediaminetet- reduced its commercial potential. Hyperaccumulators of inor- raacetic acid (EDTA) for inorganics (Raskin et al., 1997a, ganic pollutants were limited by their slow growth, low bio- Raskin, Robert and Salt, 1997b) and surfactants for organics mass and lack of suitable accumulators for some important (Johnson and Singhal, 2009) was pioneered. trace metals (Maestri and Marmiroli, 2011) while pollutant bioavailability posed challenges for the phytoremediation of However, in many cases, the solutions proposed were both organic and inorganic contaminants (Raskin et al., themselves in doubt. Biotechnology, so often seen as the long- 1997a; Raskin, Robert and Salt, 1997b). Limitations relating term solution for phytoremediation, has the limitation that to pollutants bioavailability include the following: only con- there is still substantial uncertainty surrounding biological tamination in the surface soil horizons may be removed or mechanisms that must be overcome before such biotechnolo- degraded, and clean-up is restricted to areas amenable to plant gies can be used effectively for both inorganic and organic growth. Conversely, plants may increase the bioavailability of compounds (Schwitzguébel et al., 2002; Fig. 2). The use of pollutants to the food chain, providing a potential exposure synthetic chelators is also in many cases impractical. Their pathway to accumulated pollutants (Robinson et al., 2003). use may cause unacceptable leaching, and they are expensive. −1 These drawbacks contribute to phytore mediation’s most com- The application of EDTA costs $30 000 ha to accumulate −1 monly cited limitations: the timescale and cost required for 10 g Pb kg dry weight in shoots; more readily degradable effective treatment and the safety and liability risks involved chemicals are even more expensive (Chaney et al., 2007). (Maxted et al., 2007a; Salt, Smith and Raskin, 1998). The still unresolved physical limitations of phytoremedia- At the time, solutions to many of these limitations were tion have knock-on effects for its commercialization. The proposed. As an alternative to the slow-growing hyperaccumu- length of time still required for effective phytoremediation lators, focus switched to high biomass-producing species treatments diminishes one of its most potentially attractive (Maestri and Marmiroli, 2011). Despite the effective use of advantages; its low cost as ‘time’ is viewed as an additional Figure 1. Time course of publications concerning the development of transgenic plants for phytoremediation. Closed and open bars, respectively, show the numbers of publications relating to inorganic and organic contaminants (Maestri and Marmiroli, 2011, reprinted with permission of the publisher (Taylor & Francis Ltd, http://www.tandfonline.com)). 3 Review Bioscience Horizons • Volume 7 2014 Figure 2. Mechanisms for the uptake and storage of organic and inorganic pollutants (Pilon-Smits, 2005, reprinted with permission of the publisher (Annual Reviews, http://www.annualreviews.org/)). cost in financial evaluations ( Conesa et al., 2012; Fig. 3). The offer high-potential returns (Marmiroli and McCutcheon, limited applicability of phytoremediation to the bioavailable 2004). fraction of pollutants is not taken into consideration by regu- Perceived limitations and uncertainty also detract from the lations based on traditional remediation techniques. As site- usually positive public opinion regarding phytoremediation specific risk assessments are expensive and time-consuming, due, according to the US Interstate Regulatory Council, to generic water quality standards are used, which, phytoreme- stakeholder uncertainty surrounding the fate of pollutants diation limited to the treatment of the bioavailable fraction, concentrated by plants, potentially providing entry pathways is often unable to meet (Marmiroli and McCutcheon, 2004). for pollutants into the food chain, depth of the treatment zone and the climatic and seasonal dependence of phytore- Persistent physical limitations may contribute to the fre- mediation (Marmiroli and McCutcheon, 2004). Particularly quent reports of unsuccessful or inconclusive field studies, in Europe, concerns are also associated with the potential use largely attributable to the complexity of applying techniques of genetically modified crops and the risk these may pose to developed under laboratory conditions to highly heteroge- ecosystems. As well as reducing the acceptability of phytore- neous field conditions ( Gerhardt et al., 2009). The lack of mediation, these concerns may increase its cost as sites proved reliability means that phytoremediation struggles to require greater maintenance, monitoring and disposal of attract private capital or government funding, while the small plant material due to the strict regulations relating to geneti- profit margins of dedicated phytoremediation companies are cally modified material ( Maestri and Marmiroli, 2011). insufficient to support further research. The typical source of funding for entrepreneurial start-up companies, ‘venture These limitations have been sufficient to discredit the funding’, requires newer, less, well-proven technologies to potential for phytoextraction of metals, leading Robson et al. 4 Bioscience Horizons • Volume 7 2014 Review One of the most common applications of phytotechnology which illustrates the concepts of historic applications and eco- logical engineering is the use of constructed wetlands, which may be defined as ‘shallow water with at least a 50% aerial cover of submerged or emergent macrophytes (water plants) or attached algae’ (Horne, 2000). Constructed wetlands, reed beds and floating plant systems have been used for many years to treat waste water (Cunningham, William and Huang, 1995). In 1953, the use of wetlands to reduce the over-fertilization, pollution and silting up of inland waters was suggested by Dr Kathe Seidel, inspiring the development of wetland systems in Europe and America (Hans, 1994). The application of ecologi- cal engineering is crucial as natural wetlands are inefficient in pollutant removal as water follows the shortest pathway, reduc- Figure 3. A model to evaluate the efficiency of phytoremediation. The ing the duration of treatment in the rhizosphere (Horne, 2000), period required for phytoextraction (t) is calculated as: t = A/PB where −1 whereas constructed wetlands allow the hydraulic regime, types A is the quantity of metal (mg ha ), P is the metal concentration in the −1 −1 crop (kg DM ha yr ) and B is the annual biomass production of plants and animals present, and drying cycles to be con- −1 −1 (kg DM ha yr ). Phytoextraction is modelled for the reduction of Cd trolled to maximize pollutant removal (Horne, 2000). Wetlands in the upper 0.5 m of soil; for a defined decrease in Cd content of are most important in polishing treated industrial and domestic −1 −1 1 mg kg related to soil volume and density, 8 kg C ha must be waste and removing specific pollutants, and they have focussed removed. If P and B remain constant, the required remediation period increasingly on leachate-contaminated groundwater and indus- is 15 years (Van Nevel et al., 2007, reprinted with the permission of the trial effluents ( Stottmeister et al., 2003). publisher (Elsevier, http://www.elsevier.com)). Wetlands differ from traditional phytoremediation as uptake of pollutants by plants has a secondary role. Instead, (2006) and Van Nevel et al. (2007) to conclude that this tech- their manipulation of the physiochemical environment in the nology is not yet fit for purpose, whereas phytoremediation litter and sediment layers is of greater importance, circum- of organics has achieved considerable commercial success in venting the key constraint of phytoremediation of identifying the USA (Schwitzguébel et al., 2002). or engineering appropriate plants for soil remediation (Horne, 2000). Litter from plants increases the input of Two steps back reduced carbon energy supplies for bacteria and absorption sites for inorganic cations on the COOH groups of humic Despite these limitations, phytoremediation was again saved acids (Vymazal, 2005). Hydrophytes are adapted to the from being forgotten by reincarnation within a new concept anoxic soils of wetlands and supply their roots with oxygen (Conesa et al., 2012) which built on pre-1900 practices via gas-filled channels known as aerenchyma; recorded O (McCutcheon and Schnoor, 2003) by integrating practical −1 transport rates of 126 µ mol h in Juncus ingens (giant rush) experience from agriculture, forestry and horticulture (ITRC, are of biotechnological relevance (Stottmeister et al., 2003). 2001) and recent specific chemical developments to produce Oxygen supplied by hydrophytes to their roots contributes to treatments which circumvented the traditional failings of phy- the alternating reduction states of wetlands, which are impor- toremediation and are already suitable for limited application tant for efficient removal of pollutants by both chemical and (McCutcheon and Schnoor, 2003). The term phytoremedia- microbial means (Horne, 2000). Release of oxygen by roots tion has been replaced by the concept of phytotechnology creates a steep redox gradient at the root/sediment interface, (Marmiroli, Marmiroli and Maestri, 2006), ‘the application of causing precipitation of iron, which may restrict the uptake science and engineering to examine problems and provide of toxic metals by plants due to the adsorption and immobi- solutions using plants’ (UNEP, 2003). Phytotechnology is a lization of other metals by the iron plaque (Vymazal, 2005). more overarching term (ITRC, 2001), while inclusion of the word ‘technology’ emphasizes the integration of ecological Alternating redox conditions are important for microbial engineering (UNEP, 2003) in a multidisciplinary approach processes as microbes may indirectly induce precipitation of which has been identified as being crucial for the successful iron by altering soil pH in aerobic zones, whereas microbially application of phytoremediation (Schwitzguébel, 2001). mediated sulphate reduction produces sulphide ions in anaer- Phytoremediation is now taken to mean removal or destruc- obic zones which react with metals, causing them to precipi- tion of specific contaminants by plants ( ITRC, 2001). This tate (Vymazal, 2005). Fluctuating redox states are especially definition highlights the increased use of phytostabilization, important for microbial degradation of highly chlorinated which avoids many of the limitations of phytoremediation, hydrocarbons; under the reducing conditions surrounding such as the risk of contaminants entering the food chain and macrophyte stands, highly chlorinated hydrocarbons are the inability of phytoextraction to meet regulations (Conesa degraded by reductive dehalogenation and the low-chlori- et al., 2012). Table 1 summarizes the potential application of a nated products are further degraded in the aerobic conditions range of phytotechnologies. surrounding roots and in open water (Stottmeister et al., 5 Review Bioscience Horizons • Volume 7 2014 Table 1. Applications of phytotechnology Phyto- Aim Mechanism Diagram Application technology Containment Riparian Riparian buffers Arora, Steven and James (2003) buffers for protect nearby water applied mixtures of water and runoff control resources from soil treated with three types of non-point pollution pesticide to simulate runoff to and provide bank vegetated buffer strips. They used stabilization and three replicates for each drainage habitats for aquatic treatment and buffer strip ratios and other wildlife. of 15:1 and 30:1. Sediment Their roots act as retention was 90 and 86%, filters and promote (ITRC, 2001, reprinted with permission of respectively, for the 15:1 and 30:1 microbial activity, the publisher (ITRC, http://www.itrcweb. ratio treatments. The 15:1 preventing pollutants org/)). treatment retained 53% of from entering water atrazine, 54% of metolachlor and (ITRC, 2001). 83% of chorpyrifos. Containment Infiltration caps Soil and amendments A field trial at the Lakes Creek for hydraulic act as a sponge, Landfill Site in Rockhampton, control on providing a store for Australia, involved a 5000-m landfill sites the water. Trees act as plot containing two soil depths a pump, removing (0.7 and 1.4 m), on which various water during the tree species were grown. Tree growing season. This growth, soil hydraulic character- increases the ability istics and climatic data were of the soil to retain measured and entered into the water during the HYDRUS 1D code. This simulated −1 winter, thus reducing percolation of 16.7 mm yr for the quantity of water the 1.7 m phytocap treatment −1 reaching the deeper compared with 28 mm yr at horizons by 10% of the rainfall for traditional percolation. Erosion is compacted clay caps also reduced by (Venkatraman and Ashwath, interception of rainfall 2010). by the tree canopies, and the soil binding (Venkatraman and Ashwath, 2010, reprinted effect of the root with permission of the publisher (Emerald matrix (Licht et al., Insight, http://www.emeraldinsight.com/)). 2001). Removal or Rhizosphere The role of plants is In an experiment to minimize the stabilization processes to stimulate the ecotoxicological risk of plants of growth of a accumulating pollutants during contami- beneficial microbial phytoremediation by promoting nants community in the rhizosphere processes, willow was rhizosphere. In grown hydroponically in nutrient return, microbes solution (Control) or in solutions −1 reduce the toxicity containing 500 mg L added of pollutants, dissolved organic carbon (DOC); increase or decrease both treatments contained −1 pollutant availability 25 mg L perchlorate. Tree growth and, in the case of and transpiration were similar in organics, aid their both treatments, suggesting that (ITRC, 2001, reprinted with permission of degradation any effect was microbial. the publisher (ITRC, http://www.itrcweb. (Wenzel, 2009). Perchlorate was degraded below org/)). experimental detection limits within <10 days in the added DOC treatment compared to >40 days in the control treatment. Perchlorate concentration in leaves was 5% of the initial concentration in solution in the added DOC treatment compared to 27% in the Control (Nzengung and Yifru, 2007). (Continued) 6 Bioscience Horizons • Volume 7 2014 Review Table 1. Continued Phyto - Aim Mechanism Diagram Application technology Removal or Hydroponic Plants are raised in In a joint study by Phytotech and stabilization systems for greenhouses and the International Institute of Cell of treating water exposed to Biology, sunflower plants contami- streams contaminants when (Helianthus annuus L.) were used nants (Rhizofiltration) their root systems to reduce strontium and caesium have developed. concentrations in ponds 1 km Plants are either from the Chernobyl reactor. raised on artificial Plants grown on 1 m styrofoam media through which rafts were harvested and dried contaminants are (ITRC, 2001, reprinted with permission of after 4–8 weeks to extract these passed, or suspended the publisher (ITRC, http://www.itrcweb. contaminants (Cooney, 1996). with their roots org/)). directly in the flowing water by a physical support. Plants are replaced as they become saturated with contaminants. As plants are raised in greenhouses, this method may be carried out all year (ITRC, 2001). Removal or Constructed Inorganic and Data from a marsh in Wicklow, stabilization wetlands organic contami- Ireland, were used to estimate of nants are subjected retention of dissolved metals by contami- to the range of precipitation and binding to the nants phytotechnology soil between an abandoned techniques lead/zinc mine on one side of the described in greater wetland and a lake on the other. detail in the text. In Zinc concentration in pore water subsurface decreased by 95% from −1 wetlands, water 28.5 µ mol L at the mine to −1 remains within a 1.3 µ mol L at the lake, while porous medium arsenic concentration decreased such as gravel in by 65% (Beining and Otte, 1997). beds containing The two most common types of con- only emergent structed wetland are (i) free water surface plants. Water surface wetlands and (ii) subsurface wetlands (Patel wetlands contain and Dharaiya, 2013, reprinted with sediments to permission of the publisher (Sadguru support the roots of Publications, http://www.sadgurupublica- plants covered by tions.com)). water (McCutcheon and Schnoor, 2003). Removal or Tree stands for The greater rooting In a study of phytoextraction of stabilization subsurface soil depths of trees are zinc, cadmium and copper, of and groundwa- exploited to provide contaminant uptake, root length contami- ter remediation hydraulic control and root diameter were nants (Dendrore and remediate determined for five species and mediation) deeper soil horizons related to total trace metal and contaminated concentrations in the soil. The plumes above the only tree species examined (Salix water table (ITRC, viminalis) showed good uptake 2001). efficiency for cadmium and was most effective at colonizing deep soil horizons, making it the most Root diameter distribution with depth in suitable species for tackling willow (1998) and maize (Keller et al., 2003, contamination at depths >0.7 m reprinted with permission of the publisher (Keller et al., 2003). (Springer, http://www.springer.com/)). 7 Review Bioscience Horizons • Volume 7 2014 2003; Fig. 4). Such rhizosphere processes are an important phytohydraulics, i.e. ‘the use of plants and trees to rapidly take strategy to circumvent the limitations of biotechnology and up large volumes of water in order to contain or control the synthetic chelators (Schwitzguébel, 2001; Fig. 5). migration of subsurface water’ (ITRC, 2001). The commercial success of such technologies is apparent from the patenting of Transpiration is another fundamental process exploited by the Ecolotree cap in the USA (Ecolotree, 2013), which uses phytotechnology and has been cited as the cornerstone of phy- fast-growing, deep-rooted trees to cover landfills and contami - toremediation by transporting pollutants to the shoots nated soils (Licht et al., 2001), although extensive engineering (Robinson et al., 2003); thus, mature trees can transport sub- is required for infiltration caps to succeed (Table 1). stantial quantities of pollutants to the shoots by transpiring the −1 equivalent of 810–1070 mm water yr (Licht et al., 2001). While the efficiency of conventional caps may decrease This ability to absorb water, thereby reducing runoff and with time, evapotranspiration caps are expected to become leaching of pollutants, is known as hydraulic control or increasingly effective due to root development and Figure 4. Research in the Prado Wetlands in Southern California demonstrated the successful transformation of organic compounds. Samples above and below the wetland taken for 1 year showed that halogenated peaks were common for influent water samples, while effluent had fewer halogenated peaks with a signature more similar to natural dissolved organic carbon (O’Connor-Patel and Woodside, 2004, reprinted with permission of the publisher (Orange County Water District, http://www.ocwd.com)). 8 Bioscience Horizons • Volume 7 2014 Review Figure 5. Diagrams showing the processes by which microbes may mobilize or immobilize inorganic (a) and organic (b) pollutants (Wenzel, 2009, reprinted with permission of the publisher (Springer, http://www.springer.com/)). improve ments in soil water retention resulting from litter fall. costs. The first Ecolotree phytoremediation cap was con - Evapotranspiration caps are less expensive to install than structed in 1990 at the Lakeside construction debris landfill typical prescriptive covers, and savings of $120 000– site in Oregon and 12 more have since been constructed in −1 180 000 ha have been reported, although the testing, the USA and one in Europe, in Slovenia, since 1990 (Licht modelling and monitoring of such systems may increase et al., 2001). 9 Review Bioscience Horizons • Volume 7 2014 A new focus on phytostabalization (Conesa et al., 2012) 2007). It has been suggested that, due to the low efficiency and the relatively shallow rooting depth of annual herba- relative to the land area used, phytomining will only be com- ceous plants species, whose roots typically reach a maximum mercially viable when used in conjunction with traditional depth of 50 cm (Pilon-Smits, 2005), highlights the potential mining or on contaminated soils (Robinson et al., 2009). use of trees for phytoremediation (dendroremediation). The genus Selacea produces deep tap roots with an extensive cap- Potential for phytotechnology illary fringe above the water table (Marmiroli et al., 2011), in developing countries and their large rhizosphere may reach depths of 2–3 m, facil- itating hydraulic control and increasing beneficial interac - It is estimated the global human population is increasing by tions with contaminants (Marmiroli et al., 2011; Table 1). 2.5 births every second (CIA, 2013). This, combined with increasing industrialization, will result in the remediation of contaminated soils and groundwater becoming increasingly important in rapidly developing tropical nations (Trihadinin- Phytomanagement grum, Basri and Mukhlisin, 2007). The speed of this popula- tion growth and lack of capital investment to combat Phytomanagement attempts to solve the other major limita- consequent pollution (Gerth et al., 2007) have exacerbated the tion of phytoremediation, lack of revenue (Conesa et al., lack of infrastructure for waste water and solid waste manage- 2012), by focusing on cost-efficiency or production of valu - ment (Yuen et al., 2010). Cities in the developing world are able plant biomass (Robinson et al., 2009). For example, responsible for 40% (500 m t) of global solid waste, with the dendroremediation may combine phytostabilization with most common method of disposal being to open land (Yuen enhancement of the tangible value of land (Robinson et al., et al., 2010). Water shortages are becoming an increasingly 2009), which can be increased by provision of wood, feed pressing issue, exacerbated by declining water quality (Kivaisi, products and bioenergy (Licht and Isebrands, 2005). Studies 2001). Traditional ex situ remediation technologies are gener- in the UK examined the use of short rotation willow coppice ally prohibitively expensive (Mwegoha, 2008), whereas tech- to extract Zn and Cd from soils treated with processed sew- nologies directly funded by and adopted from high-income age sludge and provided a carbon neutral energy source developed countries are often inappropriate (Yuen et al., (Maxted et al., 2007b). Phytomanagement may also be used 2010), favouring overt technologies that provide commercial to increase the intangible ecological value of land, for exam- benefits for donors ( Kivaisi, 2001). ple, the green corridor programme in the Guadiamar Valley, South West Spain (Domínguez et al., 2008). This was one of In many ways, phytotechnology appears well suited for use the largest soil remediation programmes in Europe (55 km ) in equatorial developing countries where the sustained year- and combined the aims of remediation with the creation of a round insolation enhances the photosynthesis on which phyto- continuous vegetation belt between Donana National Park technology relies to produce biomass (Trihadiningrum et al., and the Sierra Morena mountains to enhance biodiversity 2007). Most importantly, phytoremediation is a low cost tech- and facilitate animal migration (Domínguez et al., 2008). nology, making it attractive for developing countries with Another strategy to increase the economic output of phy- toremediation is selective recovery of trace metals from plant residues after they have been combusted during the process of phytomining (Schwitzguébel et al., 2002). This concept is particularly applicable to inorganic compounds, for which the perceived limitations of phytoextraction make cost an acute problem (Schwitzguébel et al., 2002). Phytomining depends on the ability of plants to accumulate economically valuable trace metals. Although there are limitations for some metals, phytomining is commercially viable for nickel, cobalt, thallium and possibly gold according to recent research (Lintern et al., 2013). Phytomining for Ni appears to show particular potential due to the number of hyperaccu- mulator species for this element which exhibit both high bio- mass production and high shoot concentrations, coupled with knowledge that the viability of phytomining depends on the financial value of the trace element involved ( Robinson et al., 2009; Fig. 6). An example of the potential importance of phytomining was presented by Li et al. (2003) who extracted Ni from Alyssum hyperaccumulator species after Figure 6. Price of nickel on the London Metal Exchange between 1985 ashing harvested biomass using an electric arc furnace, lead- and April 2007 (Chaney et al., 2007, reprinted with permission of the −1 ing to a predicted crop value of $16 000 ha (Chaney et al., publisher (ACSESS, http://www.myacsess.org/)). 10 Bioscience Horizons • Volume 7 2014 Review Table 2. Measured rainfall and drainage from phytocovers at A-ACAP trial sites (Yuen et al., 2010, reprinted with permission of the publisher) April 2007–March 2008 April 2008–March 2009 April 2009–March 2010 Mean Site Climate rainfall Rainfall Drainage Rainfall Drainage Rainfall Drainage (mm) (mm) (mm) (mm) (mm) (mm) (mm) Lyndhurst, Victoria Cool temperate 810 585 43.1 (7%) 622 3.7 (1%) 749 0.3 (<1%) McLaren Vale, Mediterranean/ 520 230 0.0 (0%) 361 0.0 (0%) 654 25.9 (4%) South Australia semi-arid limited resources (Yuen et al., 2010). The relative maturity of illustrates the potential for a methodological transfer similar the use of phytotechnology in Europe and North America has to that described by the A-Acap study of infiltration caps. led to comprehensive guidelines and recommendations for its In this study, the cost of construction of subsurface hori- creation and management which may not be directly transfer- zontal flow wetlands was similar to that of extensive treat - able to tropical environments (Kivaisi, 2001). However, ment technologies, costing US$50–100 per person. But the although the technology may not be transferred exactly due to cost of operation and maintenance was much less, just the site-specific nature of phytotechnology, it may be trans - US$2–5 per person. The study also gave examples of how ported methodologically for individual sites (Yuen et al., wetlands may be made more attractive by generating income 2010). The methodological transfer of phytotechnologies to if planted with local plant species such as elephant grass developing countries has been suggested for infiltration caps Pennisetum purpureum which may be used as animal fodder for landfill sites as these would provide many benefits, particu - or common reeds Phragmites australis which are used by larly in mitigating disposal of waste to open land; most impor- artisans to produce goods. The standard design consisted of tantly, they may cost only 35–72% of the cost of traditional a three-stage system with pre-, primary and secondary treat- covers and their repair and maintenance costs are also likely to ment stages. The secondary stage was fulfilled by the wetland be substantially less. For maximum financial economy, they which, as previously described, consisted of a waterproof should use local soils and plants. In localities where soil is not basin, filter material (litter and sediment layers), wetland ideal for phytocaps, its thickness may be manipulated with ref- plants and inlet and outlet structures. erence to local meteorological data; careful choice of indige- nous plant species that are resistant to prevailing conditions This standard system was used as a template to be applied and exploit water from the full depth of the soil profile is also in Masaya Nicatagua, San Jose las Flores, Lima Peru and important (Yuen et al., 2010). The possibility of using phyto- Pereira and Pasto Columbia. The importance of wetlands lit- caps in developing countries may be inferred from studies ter and substrate layers for the removal of pollutants was undertaken by the Australian Alternative Covers Assessment shown by the varied performance of sites using different filter Program (A-Acap) in 2007 and 2008 which included five full- media and plant species, subject to local availability. However, scale test facilities of site-specific designs across Australia, overall wetlands showed a stable treatment process, robust- spanning climates ranging from tropical in the north and arid ness and contaminant removal. The wetland scheme in Peru in the interior to temperate in the south (Yuen et al., 2010). removed over 95% of organic contamination (in terms of The results showed that, in all cases, infiltration decreased over BOD) (WSP, 2008). time, with the exception of McLaren Vale which was artifi - The scheme highlighted several other factors, in addition cially irrigated, suggesting that this technology may be applied to technical considerations for the successful application of under the varied climatic conditions necessary to make it constructed wetlands. It has been recognized that dissemina- applicable in developing countries (Table 2; Yuen et al., 2010). tion of information and local involvement is vital to encour- age the uptake of phytoremediation and ensure its As in Europe and North America, constructed wetlands sustainability (Ho, 2004). The awareness this promotes will have particular potential as a phytotechnology (Ho, 2004) increase demand for the technology and increase people’s due to their efficiency; their combination of biological, chem - willingness to pay for the systems operation and mainte- ical and physical processes; and their simple construction, nance. The importance of community involvement was made unlimited operating time and low-maintenance requirements particularly clear at the San Jose Flores wetland. This scheme (Gerth et al., 2007). was initiated by a local committee working with the Swiss The use of constructed wetlands to treat specific industrial Agency for development and Cooperation and the local contaminants in developing countries has not been well NGO Pro-Vida. Hygiene promoters, trained by the NGO, documented (Mahmood et al., 2013). However, a selection of conducted door-to-door visits ensuring that the community case studies from Latin America where constructed wetlands participated in key decisions, such as the type and location of were used to treat communities’ domestic waste, brought the wetland, encouraging active contributions to the scheme together by the water and sanitary programme (WSP, 2008) (WSP, 2008). 11 Review Bioscience Horizons • Volume 7 2014 However, it is observed that phytotechnology is not intelligent city, with the landscape and natural resources immune to limitations. Constructed Wetlands require large being important considerations during the planning process amounts of land for their implementation. The amount of (Maulan, 2014). The city includes an excellent example of land required depends on local conditions, but estimates for the successful application of constructed wetlands in a devel- the Nicaragua wetland came to 1.5 m of wetland surface oping country. The Putrajaya wetland lies in the centre of the area per person. They also require large amounts of filter and city, a 400-ha artificial lake constructed in 1997–98 to ensure liner material. If a poor choice of filter material is used, this that water quality met the required standards to permit recre- may lead to clogging that reduces the effectiveness of the ational activities. It is one of the largest freshwater wetlands scheme, requiring trained technicians to replace material. In in the tropics, involving an area of 197 ha and 12.3 m wet- Pereira Columbia, the selection of a gravel media led to fewer land plants (Trihadiningrum et al., 2007). It is hoped that instances of clogging of the filter material. To avoid limita - phytotechnologies’ incorporation of phytoremediation will tions such as this and to ensure the systems efficient removal continue to be increasingly integrated into developments, of pollutants, professional supervision over the design of wet- such as in Putrajaya, allowing continued sustainable develop- lands is crucial, highlighted by the limited control capacities ment for generations to come. of local authorities over such schemes (WSP, 2008). More generally, although phytotechnology combats many Author’s biography of the limitations of phytoremediation, its application may be Growing up on a farm in Dorset, Chloe could not fail to be constrained by the growth habit and characteristics of indi- fascinated by the natural world that surrounded her. vidual plant species, with the result that no one system is Simultaneously, it was impossible to ignore the huge effect suitable for all sites (ITRC, 2001). Thus, infiltration caps are that man was having on the landscape. These early realiza- unsuitable for areas experiencing excessive rainfall or rainfall tions influenced her BSc degree choice of Environmental so low that it cannot support plant growth (Licht et al., Science at the University of Nottingham. During her course, 2001). Wetlands may themselves become a hazard, as illus- she came to realize the complexity of the environmental trated by Keterson Marsh, USA, where a 500-ha marsh used issues involved. It became obvious that sustainable solutions to store and evaporate agricultural drainage water unknow- would only be reached if environmental goals could be ingly became contaminated with selenium that was concen- achieved while fulfilling the needs of stakeholders. For this trated in the leaves and seeds of plants, causing the death of reason, she became passionate about using our ever-increas- birds who consumed them (Horne, 2000). ing scientific knowledge to produce ecological solutions to problems which may be widely applied commercially. Chloe Conclusions hopes in future to help fulfil the potential of these technolo - gies to reduce the strain on the environment and improve the This review has considered the evolution of phytoremedia- quality of peoples’ lives. Chloe wrote this review as part of tion from initial observations of its potential to its commer- her research project in her third and final year at the University cial application today. As the fundamental properties of of Nottingham and has primary responsibility for the con- plants have essentially remained constant, this review effec- tent. She is very grateful to her co-author and supervisor tively charts the evolution of scientific thinking itself, with Colin Black, who assisted in the final write up of the paper. phytoremediation becoming simply an illustration of a much wider movement. This evolution is hinted by Lovelock (2000), who observed that the traditional bottom-up reduc- References tionist view of science is gradually progressing towards more holistic views, as seen in the transformation of phytoremedia- Alloway, J. B. (2001) Soil pollution and land contamination, in M. R. tion from the simple direct action of plants and contaminants th Chester and R. 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One step forward, two steps back: the evolution of phytoremediation into commercial technologies

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BioscienceHorizons Volume 7 2014 10.1093/biohorizons/hzu009 Review One step forward, two steps back: the evolution of phytoremediation into commercial technologies Chloe Stephenson* and Colin R. Black School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK *Corresponding author: Tel: +44 07909912125. Email: stepcj@hotmail.co.uk Supervisor: Colin R. Black, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK. Tel: +44 01159516337. Email: colin.black@nottingham.ac.uk This review charts the evolution of phytoremediation from its earliest beginnings, with the discovery of metal tolerant plants in the 16th century and metabolism of organic pollutants by plants in the 1940s. The rapid expansion of research in the early 1990s led to many crucial discoveries but failed to surmount the fundamental limitations that often impede commercial appli- cation of phytoremediation. It is argued that phytoremediation was saved from being forgotten by its evolution under the new term phytotechnology, or ‘the application of science and engineering to examine problems and provide solutions using plants’. This review explores the use of phytotechnology for ecological engineering using constructed wetlands and evapo- transpiration caps as landfill covers. Finally, the transfer of phytotechnology to developing countries, where it has great potential to solve the growing problem of pollution, is examined. The development of phytotechnology can be perceived as an illustration of the modern evolution of scientific thought, from the traditional reductionist view to a wider holistic approach which takes into account the natural environment and our need to preserve it. It is hoped that the evolution of both will allow for increasing conservation of finite resources without sacrificing continued development. Key words: phytoextraction, phytoremediation, phytomining, phytotechnologies, structured wetlands, infiltration caps Submitted on 6 January 2014; accepted on 21 August 2014 Introduction Disposal of industrial waste was previously regarded as a non-productive function to be achieved at least possible cost The Oxford Dictionary (2013) defines a paradigmatic shift as (Hamlin, 2002). In the race for progress and prosperity, this led ‘a fundamental change in approach or underlying assump- to extensive pollution, causing the Global Assessment of Soil tions’. Such shifts occur as evidence accumulates to dispute Degradation to estimate that 21.8 × 10 ha of land in Europe, old ideas and support new ones (Kuhn, 2012), and may argu- Asia, Africa and Central America was affected by chemical pol- ably have occurred in the way humanity views the natural lutants (Alloway, 2001). Chemical pollution of soil may involve environment; a widely cited origin for such a shift is Rachel both inorganic and organic compounds. The former include Carson’s (1962) book, ‘A Silent Spring’, which recognized trace metals, which occur naturally in all soils, but whose con- the complex and vital role of soil in regulating the biosphere, centration may increase following release from diverse anthro- ‘the thin layer of soil that forms a patchy covering over the pogenic sources including metalliferous mining, smelting and continents [which] controls our own existence and that of waste disposal (Alloway, 2001). Two important categories of every other animal of the land’. This was soon followed by pollutants containing organic hydrocarbons include a range of the development of the Gaia principle, which proposed that saturated alkenes and organic components containing nitrogen, living organisms interact with their abiotic environment to sulphur and aromatic hydrocarbons from petroleum and persis- establish complex systems that contribute to maintenance of tent organic pollutants, which are arbitrarily classified as life on Earth (Lovelock, 1967, 2000). ‘organic compounds that are resistant to environmental © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Review Bioscience Horizons • Volume 7 2014 degradation through chemical, biological and photolytic pro- discovered in the 16th Century by Andrea Cesalpino (Brooks, cesses’ (Stockholm Convention, 2008). The definition has been 1998). Realization of the implications of these observations extended to include polycyclic aromatic hydrocarbons and poly- was slow until in 1940 Miller showed that the metabolism of chlorinated biphenyls among others (Alloway, 2001). xenobiotics infused into intact plants was analogous to their transformation and conjugation in mammals (Sandermann, Recognition of the threat posed by pollution in the USA 1994). Margazzi and Vergano (1948) reported the accumula- forced changes in legislation (Hamlin, 2002). The 1965 tion of nickel (Ni) in Alyssum bertolonnii to concentrations of Waste Disposal Act was the first to regulate waste on a upto 0.79% from soil containing 0.42% Ni (Brooks, 1998). national scale and was followed by the creation of the Environmental Protection Agency (EPA) by President Nixon However, ignorance of these findings led to the view that in 1970. The fines and penalties imposed transformed waste phytoremediation was impossible as it was assumed that high disposal from a non-productive function to a productive ven- soil metal concentrations induced matrix toxicity (McCutcheon ture and initiated the search for efficient, cost-effective reme - and Schnoor, 2003), and that plants could not metabolize non- diation technologies for cleaning contaminated sites. Various polar xenobiotics such as the organochlorine insecticide, technologies were developed that focused on stabilization dichlorodiphenyltrichloroethane (DDT; Russell, 2005); these (permeable reactive barriers) or removal (excavation and views were subsequently discredited for both organic and inor- landfill) of pollutants; their primary disadvantage was that ganic compounds. The feasibility of degrading organics was they were clumsy, costly and inefficient ( Hamlin, 2002). elucidated in the ‘green liver model’ of organic metabolism by plants (Sandermann, 1994) and proved by studies of An emerging alternative is phytoremediation, ‘the use of Petroselinium hortense which demonstrated its ability to green plant-based systems to remediate contaminated soils, degrade DDT (Russell, 2005). For inorganic pollutants, the sediments and water’ (Kruger, Todd and Joel, 1997). metal-tolerant species first observed by Andrea Cesalpino were Phytoremediation has the advantage that it may remediate rediscovered by Brooks et al. (1977) who coined the term, soils similarly to traditional techniques, removing or stabiliz- hyperaccumulator, to describe plants able to accumulate 0.1% ing contaminants but, as it relies on plant physiological pro- Ni in dry matter, 100 times greater than the concentrations cesses, is solar-driven and so is typically 10-fold cheaper tolerated by non-accumulator plants (Brooks, 1998), solving (Pilon-Smits, 2005). Another advantage is that phytoremedi- the problem of matrix toxicity. ation is carried out in situ, contributing to its relatively low cost and limiting human and environmental exposure to pol- These discoveries led to realization of the potential of phy- lutants; phytoremediation is popular, because it is perceived toremediation, and rapid advances were made in the early as a clean green technology. This review examines the evolu- 1990s, cemented by the filing of a Japanese patent by tion of phytoremediation of industrial pollutants into a Utsunomiya for the use of plants to extract Cd (McCutcheon widely applicable and commercial technology and reveals its and Rock, 2001). untapped potential for use in developing tropical countries. One step back One step forward Differing research approaches led to a varied uptake of com- mercial phytoremediation in its two largest markets, Europe Although phytoremediation is often described as a ‘new’ and America. In America, funding by organizations such as the technology, this is incorrect as it has arguably evolved over Environmental Protection Agency (EPA) and the Department the past 300 years due to developments in land reclamation, of Defence encouraged application-based research, focusing land farming of oily wastes and improved herbicide, pesticide on real-life contamination scenarios. This resulted in the rela- and agronomic technologies (McCutcheon and Rock, 2001). tive success of commercial phytoremediation, as entrepreneur- During this progression, the fundamental principle of using ial businesses attached to research institutes quickly sprang up. plants for environmental remediation has remained constant, An example of such a company is illustrated later in this arti- but changing paradigms of technology and understanding cle, in Ecolotree’s use of trees on landfill sites ( Ecolotree, 2013). have been superimposed. In contrast, European schemes focusing on fundamental Phytoextraction of trace metals initially received far greater research such as the COST Action 837 have resulted in the attention than organic compounds due to the difficulty of limited success of commercial phytoremediation projects analysing the latter and their transformations (Watanabe, (Schwitzguébel et al., 2002). 1997). However, the origin of both technologies was similar, stemming from early observations of unusual interactions The widely cited report by Glass (1999) captured the prevail- between plants and their environment; for organics, this orig- ing optimism regarding commercialization of phytoremediation inated from observations that concentrations of these pollut- in the USA by reporting that the potential global market for this −1 ants decreased more rapidly in vegetated soils (Salt, Smith and technology had increased from $15–18 bn yr in 1998 to $34– −1 Raskin, 1998). For inorganics, distinctive plant communities 54 bn yr in 1999, predicting that the US market would reach known as serpentine vegetation were identified growing on $235–400 million by 2005. However, the review by Pilon-Smits ultramafic soils with a high Mg and Fe content, as first (2005) included a personal communication from Glass stating 2 Bioscience Horizons • Volume 7 2014 Review that the US phytoremediation market was worth $100–150 mil- traditional breeding techniques to improve plants for lion at that time, and Conesa et al. (2012) observed that ‘virtu- phytoremediaton, particularly for complete degradation of ally none of this potential materialized in the subsequent decade’. organic pollutants by plants (Van Aken, 2008), it soon became This suggests that phytoremediation has not achieved its pre- clear that biotechnology would have a major role in elucidating dicted potential as a commercial technology. biological mechanisms and providing novel genetic material. The first papers detailing the use of transgenics in phytoreme - Phytoremediation is arguably trapped in a vicious cycle diation involved the introduction of a human metallothionein where uncertainty, an affliction of all innovative new tech - into Nicotiana tobaccum L. (tobacco) to increase Cd accumula- nologies (Glass, 1999), discourages the funding required to tion and rabbit esterase in Solanum lycopersicum L. (tomato) finance further research. With the result that phytoremedia - to provide resistance to the herbicide, thiazopyr (Maestri and tion’s limitations remain unsolved. Marmiroli, 2011; Fig. 1). During its development, phytoremediation encountered To solve the problem of bioavailability, the use of soil several fundamental physical limitations of plants which amendments, including chelates such as ethylenediaminetet- reduced its commercial potential. Hyperaccumulators of inor- raacetic acid (EDTA) for inorganics (Raskin et al., 1997a, ganic pollutants were limited by their slow growth, low bio- Raskin, Robert and Salt, 1997b) and surfactants for organics mass and lack of suitable accumulators for some important (Johnson and Singhal, 2009) was pioneered. trace metals (Maestri and Marmiroli, 2011) while pollutant bioavailability posed challenges for the phytoremediation of However, in many cases, the solutions proposed were both organic and inorganic contaminants (Raskin et al., themselves in doubt. Biotechnology, so often seen as the long- 1997a; Raskin, Robert and Salt, 1997b). Limitations relating term solution for phytoremediation, has the limitation that to pollutants bioavailability include the following: only con- there is still substantial uncertainty surrounding biological tamination in the surface soil horizons may be removed or mechanisms that must be overcome before such biotechnolo- degraded, and clean-up is restricted to areas amenable to plant gies can be used effectively for both inorganic and organic growth. Conversely, plants may increase the bioavailability of compounds (Schwitzguébel et al., 2002; Fig. 2). The use of pollutants to the food chain, providing a potential exposure synthetic chelators is also in many cases impractical. Their pathway to accumulated pollutants (Robinson et al., 2003). use may cause unacceptable leaching, and they are expensive. −1 These drawbacks contribute to phytore mediation’s most com- The application of EDTA costs $30 000 ha to accumulate −1 monly cited limitations: the timescale and cost required for 10 g Pb kg dry weight in shoots; more readily degradable effective treatment and the safety and liability risks involved chemicals are even more expensive (Chaney et al., 2007). (Maxted et al., 2007a; Salt, Smith and Raskin, 1998). The still unresolved physical limitations of phytoremedia- At the time, solutions to many of these limitations were tion have knock-on effects for its commercialization. The proposed. As an alternative to the slow-growing hyperaccumu- length of time still required for effective phytoremediation lators, focus switched to high biomass-producing species treatments diminishes one of its most potentially attractive (Maestri and Marmiroli, 2011). Despite the effective use of advantages; its low cost as ‘time’ is viewed as an additional Figure 1. Time course of publications concerning the development of transgenic plants for phytoremediation. Closed and open bars, respectively, show the numbers of publications relating to inorganic and organic contaminants (Maestri and Marmiroli, 2011, reprinted with permission of the publisher (Taylor & Francis Ltd, http://www.tandfonline.com)). 3 Review Bioscience Horizons • Volume 7 2014 Figure 2. Mechanisms for the uptake and storage of organic and inorganic pollutants (Pilon-Smits, 2005, reprinted with permission of the publisher (Annual Reviews, http://www.annualreviews.org/)). cost in financial evaluations ( Conesa et al., 2012; Fig. 3). The offer high-potential returns (Marmiroli and McCutcheon, limited applicability of phytoremediation to the bioavailable 2004). fraction of pollutants is not taken into consideration by regu- Perceived limitations and uncertainty also detract from the lations based on traditional remediation techniques. As site- usually positive public opinion regarding phytoremediation specific risk assessments are expensive and time-consuming, due, according to the US Interstate Regulatory Council, to generic water quality standards are used, which, phytoreme- stakeholder uncertainty surrounding the fate of pollutants diation limited to the treatment of the bioavailable fraction, concentrated by plants, potentially providing entry pathways is often unable to meet (Marmiroli and McCutcheon, 2004). for pollutants into the food chain, depth of the treatment zone and the climatic and seasonal dependence of phytore- Persistent physical limitations may contribute to the fre- mediation (Marmiroli and McCutcheon, 2004). Particularly quent reports of unsuccessful or inconclusive field studies, in Europe, concerns are also associated with the potential use largely attributable to the complexity of applying techniques of genetically modified crops and the risk these may pose to developed under laboratory conditions to highly heteroge- ecosystems. As well as reducing the acceptability of phytore- neous field conditions ( Gerhardt et al., 2009). The lack of mediation, these concerns may increase its cost as sites proved reliability means that phytoremediation struggles to require greater maintenance, monitoring and disposal of attract private capital or government funding, while the small plant material due to the strict regulations relating to geneti- profit margins of dedicated phytoremediation companies are cally modified material ( Maestri and Marmiroli, 2011). insufficient to support further research. The typical source of funding for entrepreneurial start-up companies, ‘venture These limitations have been sufficient to discredit the funding’, requires newer, less, well-proven technologies to potential for phytoextraction of metals, leading Robson et al. 4 Bioscience Horizons • Volume 7 2014 Review One of the most common applications of phytotechnology which illustrates the concepts of historic applications and eco- logical engineering is the use of constructed wetlands, which may be defined as ‘shallow water with at least a 50% aerial cover of submerged or emergent macrophytes (water plants) or attached algae’ (Horne, 2000). Constructed wetlands, reed beds and floating plant systems have been used for many years to treat waste water (Cunningham, William and Huang, 1995). In 1953, the use of wetlands to reduce the over-fertilization, pollution and silting up of inland waters was suggested by Dr Kathe Seidel, inspiring the development of wetland systems in Europe and America (Hans, 1994). The application of ecologi- cal engineering is crucial as natural wetlands are inefficient in pollutant removal as water follows the shortest pathway, reduc- Figure 3. A model to evaluate the efficiency of phytoremediation. The ing the duration of treatment in the rhizosphere (Horne, 2000), period required for phytoextraction (t) is calculated as: t = A/PB where −1 whereas constructed wetlands allow the hydraulic regime, types A is the quantity of metal (mg ha ), P is the metal concentration in the −1 −1 crop (kg DM ha yr ) and B is the annual biomass production of plants and animals present, and drying cycles to be con- −1 −1 (kg DM ha yr ). Phytoextraction is modelled for the reduction of Cd trolled to maximize pollutant removal (Horne, 2000). Wetlands in the upper 0.5 m of soil; for a defined decrease in Cd content of are most important in polishing treated industrial and domestic −1 −1 1 mg kg related to soil volume and density, 8 kg C ha must be waste and removing specific pollutants, and they have focussed removed. If P and B remain constant, the required remediation period increasingly on leachate-contaminated groundwater and indus- is 15 years (Van Nevel et al., 2007, reprinted with the permission of the trial effluents ( Stottmeister et al., 2003). publisher (Elsevier, http://www.elsevier.com)). Wetlands differ from traditional phytoremediation as uptake of pollutants by plants has a secondary role. Instead, (2006) and Van Nevel et al. (2007) to conclude that this tech- their manipulation of the physiochemical environment in the nology is not yet fit for purpose, whereas phytoremediation litter and sediment layers is of greater importance, circum- of organics has achieved considerable commercial success in venting the key constraint of phytoremediation of identifying the USA (Schwitzguébel et al., 2002). or engineering appropriate plants for soil remediation (Horne, 2000). Litter from plants increases the input of Two steps back reduced carbon energy supplies for bacteria and absorption sites for inorganic cations on the COOH groups of humic Despite these limitations, phytoremediation was again saved acids (Vymazal, 2005). Hydrophytes are adapted to the from being forgotten by reincarnation within a new concept anoxic soils of wetlands and supply their roots with oxygen (Conesa et al., 2012) which built on pre-1900 practices via gas-filled channels known as aerenchyma; recorded O (McCutcheon and Schnoor, 2003) by integrating practical −1 transport rates of 126 µ mol h in Juncus ingens (giant rush) experience from agriculture, forestry and horticulture (ITRC, are of biotechnological relevance (Stottmeister et al., 2003). 2001) and recent specific chemical developments to produce Oxygen supplied by hydrophytes to their roots contributes to treatments which circumvented the traditional failings of phy- the alternating reduction states of wetlands, which are impor- toremediation and are already suitable for limited application tant for efficient removal of pollutants by both chemical and (McCutcheon and Schnoor, 2003). The term phytoremedia- microbial means (Horne, 2000). Release of oxygen by roots tion has been replaced by the concept of phytotechnology creates a steep redox gradient at the root/sediment interface, (Marmiroli, Marmiroli and Maestri, 2006), ‘the application of causing precipitation of iron, which may restrict the uptake science and engineering to examine problems and provide of toxic metals by plants due to the adsorption and immobi- solutions using plants’ (UNEP, 2003). Phytotechnology is a lization of other metals by the iron plaque (Vymazal, 2005). more overarching term (ITRC, 2001), while inclusion of the word ‘technology’ emphasizes the integration of ecological Alternating redox conditions are important for microbial engineering (UNEP, 2003) in a multidisciplinary approach processes as microbes may indirectly induce precipitation of which has been identified as being crucial for the successful iron by altering soil pH in aerobic zones, whereas microbially application of phytoremediation (Schwitzguébel, 2001). mediated sulphate reduction produces sulphide ions in anaer- Phytoremediation is now taken to mean removal or destruc- obic zones which react with metals, causing them to precipi- tion of specific contaminants by plants ( ITRC, 2001). This tate (Vymazal, 2005). Fluctuating redox states are especially definition highlights the increased use of phytostabilization, important for microbial degradation of highly chlorinated which avoids many of the limitations of phytoremediation, hydrocarbons; under the reducing conditions surrounding such as the risk of contaminants entering the food chain and macrophyte stands, highly chlorinated hydrocarbons are the inability of phytoextraction to meet regulations (Conesa degraded by reductive dehalogenation and the low-chlori- et al., 2012). Table 1 summarizes the potential application of a nated products are further degraded in the aerobic conditions range of phytotechnologies. surrounding roots and in open water (Stottmeister et al., 5 Review Bioscience Horizons • Volume 7 2014 Table 1. Applications of phytotechnology Phyto- Aim Mechanism Diagram Application technology Containment Riparian Riparian buffers Arora, Steven and James (2003) buffers for protect nearby water applied mixtures of water and runoff control resources from soil treated with three types of non-point pollution pesticide to simulate runoff to and provide bank vegetated buffer strips. They used stabilization and three replicates for each drainage habitats for aquatic treatment and buffer strip ratios and other wildlife. of 15:1 and 30:1. Sediment Their roots act as retention was 90 and 86%, filters and promote (ITRC, 2001, reprinted with permission of respectively, for the 15:1 and 30:1 microbial activity, the publisher (ITRC, http://www.itrcweb. ratio treatments. The 15:1 preventing pollutants org/)). treatment retained 53% of from entering water atrazine, 54% of metolachlor and (ITRC, 2001). 83% of chorpyrifos. Containment Infiltration caps Soil and amendments A field trial at the Lakes Creek for hydraulic act as a sponge, Landfill Site in Rockhampton, control on providing a store for Australia, involved a 5000-m landfill sites the water. Trees act as plot containing two soil depths a pump, removing (0.7 and 1.4 m), on which various water during the tree species were grown. Tree growing season. This growth, soil hydraulic character- increases the ability istics and climatic data were of the soil to retain measured and entered into the water during the HYDRUS 1D code. This simulated −1 winter, thus reducing percolation of 16.7 mm yr for the quantity of water the 1.7 m phytocap treatment −1 reaching the deeper compared with 28 mm yr at horizons by 10% of the rainfall for traditional percolation. Erosion is compacted clay caps also reduced by (Venkatraman and Ashwath, interception of rainfall 2010). by the tree canopies, and the soil binding (Venkatraman and Ashwath, 2010, reprinted effect of the root with permission of the publisher (Emerald matrix (Licht et al., Insight, http://www.emeraldinsight.com/)). 2001). Removal or Rhizosphere The role of plants is In an experiment to minimize the stabilization processes to stimulate the ecotoxicological risk of plants of growth of a accumulating pollutants during contami- beneficial microbial phytoremediation by promoting nants community in the rhizosphere processes, willow was rhizosphere. In grown hydroponically in nutrient return, microbes solution (Control) or in solutions −1 reduce the toxicity containing 500 mg L added of pollutants, dissolved organic carbon (DOC); increase or decrease both treatments contained −1 pollutant availability 25 mg L perchlorate. Tree growth and, in the case of and transpiration were similar in organics, aid their both treatments, suggesting that (ITRC, 2001, reprinted with permission of degradation any effect was microbial. the publisher (ITRC, http://www.itrcweb. (Wenzel, 2009). Perchlorate was degraded below org/)). experimental detection limits within <10 days in the added DOC treatment compared to >40 days in the control treatment. Perchlorate concentration in leaves was 5% of the initial concentration in solution in the added DOC treatment compared to 27% in the Control (Nzengung and Yifru, 2007). (Continued) 6 Bioscience Horizons • Volume 7 2014 Review Table 1. Continued Phyto - Aim Mechanism Diagram Application technology Removal or Hydroponic Plants are raised in In a joint study by Phytotech and stabilization systems for greenhouses and the International Institute of Cell of treating water exposed to Biology, sunflower plants contami- streams contaminants when (Helianthus annuus L.) were used nants (Rhizofiltration) their root systems to reduce strontium and caesium have developed. concentrations in ponds 1 km Plants are either from the Chernobyl reactor. raised on artificial Plants grown on 1 m styrofoam media through which rafts were harvested and dried contaminants are (ITRC, 2001, reprinted with permission of after 4–8 weeks to extract these passed, or suspended the publisher (ITRC, http://www.itrcweb. contaminants (Cooney, 1996). with their roots org/)). directly in the flowing water by a physical support. Plants are replaced as they become saturated with contaminants. As plants are raised in greenhouses, this method may be carried out all year (ITRC, 2001). Removal or Constructed Inorganic and Data from a marsh in Wicklow, stabilization wetlands organic contami- Ireland, were used to estimate of nants are subjected retention of dissolved metals by contami- to the range of precipitation and binding to the nants phytotechnology soil between an abandoned techniques lead/zinc mine on one side of the described in greater wetland and a lake on the other. detail in the text. In Zinc concentration in pore water subsurface decreased by 95% from −1 wetlands, water 28.5 µ mol L at the mine to −1 remains within a 1.3 µ mol L at the lake, while porous medium arsenic concentration decreased such as gravel in by 65% (Beining and Otte, 1997). beds containing The two most common types of con- only emergent structed wetland are (i) free water surface plants. Water surface wetlands and (ii) subsurface wetlands (Patel wetlands contain and Dharaiya, 2013, reprinted with sediments to permission of the publisher (Sadguru support the roots of Publications, http://www.sadgurupublica- plants covered by tions.com)). water (McCutcheon and Schnoor, 2003). Removal or Tree stands for The greater rooting In a study of phytoextraction of stabilization subsurface soil depths of trees are zinc, cadmium and copper, of and groundwa- exploited to provide contaminant uptake, root length contami- ter remediation hydraulic control and root diameter were nants (Dendrore and remediate determined for five species and mediation) deeper soil horizons related to total trace metal and contaminated concentrations in the soil. The plumes above the only tree species examined (Salix water table (ITRC, viminalis) showed good uptake 2001). efficiency for cadmium and was most effective at colonizing deep soil horizons, making it the most Root diameter distribution with depth in suitable species for tackling willow (1998) and maize (Keller et al., 2003, contamination at depths >0.7 m reprinted with permission of the publisher (Keller et al., 2003). (Springer, http://www.springer.com/)). 7 Review Bioscience Horizons • Volume 7 2014 2003; Fig. 4). Such rhizosphere processes are an important phytohydraulics, i.e. ‘the use of plants and trees to rapidly take strategy to circumvent the limitations of biotechnology and up large volumes of water in order to contain or control the synthetic chelators (Schwitzguébel, 2001; Fig. 5). migration of subsurface water’ (ITRC, 2001). The commercial success of such technologies is apparent from the patenting of Transpiration is another fundamental process exploited by the Ecolotree cap in the USA (Ecolotree, 2013), which uses phytotechnology and has been cited as the cornerstone of phy- fast-growing, deep-rooted trees to cover landfills and contami - toremediation by transporting pollutants to the shoots nated soils (Licht et al., 2001), although extensive engineering (Robinson et al., 2003); thus, mature trees can transport sub- is required for infiltration caps to succeed (Table 1). stantial quantities of pollutants to the shoots by transpiring the −1 equivalent of 810–1070 mm water yr (Licht et al., 2001). While the efficiency of conventional caps may decrease This ability to absorb water, thereby reducing runoff and with time, evapotranspiration caps are expected to become leaching of pollutants, is known as hydraulic control or increasingly effective due to root development and Figure 4. Research in the Prado Wetlands in Southern California demonstrated the successful transformation of organic compounds. Samples above and below the wetland taken for 1 year showed that halogenated peaks were common for influent water samples, while effluent had fewer halogenated peaks with a signature more similar to natural dissolved organic carbon (O’Connor-Patel and Woodside, 2004, reprinted with permission of the publisher (Orange County Water District, http://www.ocwd.com)). 8 Bioscience Horizons • Volume 7 2014 Review Figure 5. Diagrams showing the processes by which microbes may mobilize or immobilize inorganic (a) and organic (b) pollutants (Wenzel, 2009, reprinted with permission of the publisher (Springer, http://www.springer.com/)). improve ments in soil water retention resulting from litter fall. costs. The first Ecolotree phytoremediation cap was con - Evapotranspiration caps are less expensive to install than structed in 1990 at the Lakeside construction debris landfill typical prescriptive covers, and savings of $120 000– site in Oregon and 12 more have since been constructed in −1 180 000 ha have been reported, although the testing, the USA and one in Europe, in Slovenia, since 1990 (Licht modelling and monitoring of such systems may increase et al., 2001). 9 Review Bioscience Horizons • Volume 7 2014 A new focus on phytostabalization (Conesa et al., 2012) 2007). It has been suggested that, due to the low efficiency and the relatively shallow rooting depth of annual herba- relative to the land area used, phytomining will only be com- ceous plants species, whose roots typically reach a maximum mercially viable when used in conjunction with traditional depth of 50 cm (Pilon-Smits, 2005), highlights the potential mining or on contaminated soils (Robinson et al., 2009). use of trees for phytoremediation (dendroremediation). The genus Selacea produces deep tap roots with an extensive cap- Potential for phytotechnology illary fringe above the water table (Marmiroli et al., 2011), in developing countries and their large rhizosphere may reach depths of 2–3 m, facil- itating hydraulic control and increasing beneficial interac - It is estimated the global human population is increasing by tions with contaminants (Marmiroli et al., 2011; Table 1). 2.5 births every second (CIA, 2013). This, combined with increasing industrialization, will result in the remediation of contaminated soils and groundwater becoming increasingly important in rapidly developing tropical nations (Trihadinin- Phytomanagement grum, Basri and Mukhlisin, 2007). The speed of this popula- tion growth and lack of capital investment to combat Phytomanagement attempts to solve the other major limita- consequent pollution (Gerth et al., 2007) have exacerbated the tion of phytoremediation, lack of revenue (Conesa et al., lack of infrastructure for waste water and solid waste manage- 2012), by focusing on cost-efficiency or production of valu - ment (Yuen et al., 2010). Cities in the developing world are able plant biomass (Robinson et al., 2009). For example, responsible for 40% (500 m t) of global solid waste, with the dendroremediation may combine phytostabilization with most common method of disposal being to open land (Yuen enhancement of the tangible value of land (Robinson et al., et al., 2010). Water shortages are becoming an increasingly 2009), which can be increased by provision of wood, feed pressing issue, exacerbated by declining water quality (Kivaisi, products and bioenergy (Licht and Isebrands, 2005). Studies 2001). Traditional ex situ remediation technologies are gener- in the UK examined the use of short rotation willow coppice ally prohibitively expensive (Mwegoha, 2008), whereas tech- to extract Zn and Cd from soils treated with processed sew- nologies directly funded by and adopted from high-income age sludge and provided a carbon neutral energy source developed countries are often inappropriate (Yuen et al., (Maxted et al., 2007b). Phytomanagement may also be used 2010), favouring overt technologies that provide commercial to increase the intangible ecological value of land, for exam- benefits for donors ( Kivaisi, 2001). ple, the green corridor programme in the Guadiamar Valley, South West Spain (Domínguez et al., 2008). This was one of In many ways, phytotechnology appears well suited for use the largest soil remediation programmes in Europe (55 km ) in equatorial developing countries where the sustained year- and combined the aims of remediation with the creation of a round insolation enhances the photosynthesis on which phyto- continuous vegetation belt between Donana National Park technology relies to produce biomass (Trihadiningrum et al., and the Sierra Morena mountains to enhance biodiversity 2007). Most importantly, phytoremediation is a low cost tech- and facilitate animal migration (Domínguez et al., 2008). nology, making it attractive for developing countries with Another strategy to increase the economic output of phy- toremediation is selective recovery of trace metals from plant residues after they have been combusted during the process of phytomining (Schwitzguébel et al., 2002). This concept is particularly applicable to inorganic compounds, for which the perceived limitations of phytoextraction make cost an acute problem (Schwitzguébel et al., 2002). Phytomining depends on the ability of plants to accumulate economically valuable trace metals. Although there are limitations for some metals, phytomining is commercially viable for nickel, cobalt, thallium and possibly gold according to recent research (Lintern et al., 2013). Phytomining for Ni appears to show particular potential due to the number of hyperaccu- mulator species for this element which exhibit both high bio- mass production and high shoot concentrations, coupled with knowledge that the viability of phytomining depends on the financial value of the trace element involved ( Robinson et al., 2009; Fig. 6). An example of the potential importance of phytomining was presented by Li et al. (2003) who extracted Ni from Alyssum hyperaccumulator species after Figure 6. Price of nickel on the London Metal Exchange between 1985 ashing harvested biomass using an electric arc furnace, lead- and April 2007 (Chaney et al., 2007, reprinted with permission of the −1 ing to a predicted crop value of $16 000 ha (Chaney et al., publisher (ACSESS, http://www.myacsess.org/)). 10 Bioscience Horizons • Volume 7 2014 Review Table 2. Measured rainfall and drainage from phytocovers at A-ACAP trial sites (Yuen et al., 2010, reprinted with permission of the publisher) April 2007–March 2008 April 2008–March 2009 April 2009–March 2010 Mean Site Climate rainfall Rainfall Drainage Rainfall Drainage Rainfall Drainage (mm) (mm) (mm) (mm) (mm) (mm) (mm) Lyndhurst, Victoria Cool temperate 810 585 43.1 (7%) 622 3.7 (1%) 749 0.3 (<1%) McLaren Vale, Mediterranean/ 520 230 0.0 (0%) 361 0.0 (0%) 654 25.9 (4%) South Australia semi-arid limited resources (Yuen et al., 2010). The relative maturity of illustrates the potential for a methodological transfer similar the use of phytotechnology in Europe and North America has to that described by the A-Acap study of infiltration caps. led to comprehensive guidelines and recommendations for its In this study, the cost of construction of subsurface hori- creation and management which may not be directly transfer- zontal flow wetlands was similar to that of extensive treat - able to tropical environments (Kivaisi, 2001). However, ment technologies, costing US$50–100 per person. But the although the technology may not be transferred exactly due to cost of operation and maintenance was much less, just the site-specific nature of phytotechnology, it may be trans - US$2–5 per person. The study also gave examples of how ported methodologically for individual sites (Yuen et al., wetlands may be made more attractive by generating income 2010). The methodological transfer of phytotechnologies to if planted with local plant species such as elephant grass developing countries has been suggested for infiltration caps Pennisetum purpureum which may be used as animal fodder for landfill sites as these would provide many benefits, particu - or common reeds Phragmites australis which are used by larly in mitigating disposal of waste to open land; most impor- artisans to produce goods. The standard design consisted of tantly, they may cost only 35–72% of the cost of traditional a three-stage system with pre-, primary and secondary treat- covers and their repair and maintenance costs are also likely to ment stages. The secondary stage was fulfilled by the wetland be substantially less. For maximum financial economy, they which, as previously described, consisted of a waterproof should use local soils and plants. In localities where soil is not basin, filter material (litter and sediment layers), wetland ideal for phytocaps, its thickness may be manipulated with ref- plants and inlet and outlet structures. erence to local meteorological data; careful choice of indige- nous plant species that are resistant to prevailing conditions This standard system was used as a template to be applied and exploit water from the full depth of the soil profile is also in Masaya Nicatagua, San Jose las Flores, Lima Peru and important (Yuen et al., 2010). The possibility of using phyto- Pereira and Pasto Columbia. The importance of wetlands lit- caps in developing countries may be inferred from studies ter and substrate layers for the removal of pollutants was undertaken by the Australian Alternative Covers Assessment shown by the varied performance of sites using different filter Program (A-Acap) in 2007 and 2008 which included five full- media and plant species, subject to local availability. However, scale test facilities of site-specific designs across Australia, overall wetlands showed a stable treatment process, robust- spanning climates ranging from tropical in the north and arid ness and contaminant removal. The wetland scheme in Peru in the interior to temperate in the south (Yuen et al., 2010). removed over 95% of organic contamination (in terms of The results showed that, in all cases, infiltration decreased over BOD) (WSP, 2008). time, with the exception of McLaren Vale which was artifi - The scheme highlighted several other factors, in addition cially irrigated, suggesting that this technology may be applied to technical considerations for the successful application of under the varied climatic conditions necessary to make it constructed wetlands. It has been recognized that dissemina- applicable in developing countries (Table 2; Yuen et al., 2010). tion of information and local involvement is vital to encour- age the uptake of phytoremediation and ensure its As in Europe and North America, constructed wetlands sustainability (Ho, 2004). The awareness this promotes will have particular potential as a phytotechnology (Ho, 2004) increase demand for the technology and increase people’s due to their efficiency; their combination of biological, chem - willingness to pay for the systems operation and mainte- ical and physical processes; and their simple construction, nance. The importance of community involvement was made unlimited operating time and low-maintenance requirements particularly clear at the San Jose Flores wetland. This scheme (Gerth et al., 2007). was initiated by a local committee working with the Swiss The use of constructed wetlands to treat specific industrial Agency for development and Cooperation and the local contaminants in developing countries has not been well NGO Pro-Vida. Hygiene promoters, trained by the NGO, documented (Mahmood et al., 2013). However, a selection of conducted door-to-door visits ensuring that the community case studies from Latin America where constructed wetlands participated in key decisions, such as the type and location of were used to treat communities’ domestic waste, brought the wetland, encouraging active contributions to the scheme together by the water and sanitary programme (WSP, 2008) (WSP, 2008). 11 Review Bioscience Horizons • Volume 7 2014 However, it is observed that phytotechnology is not intelligent city, with the landscape and natural resources immune to limitations. Constructed Wetlands require large being important considerations during the planning process amounts of land for their implementation. The amount of (Maulan, 2014). The city includes an excellent example of land required depends on local conditions, but estimates for the successful application of constructed wetlands in a devel- the Nicaragua wetland came to 1.5 m of wetland surface oping country. The Putrajaya wetland lies in the centre of the area per person. They also require large amounts of filter and city, a 400-ha artificial lake constructed in 1997–98 to ensure liner material. If a poor choice of filter material is used, this that water quality met the required standards to permit recre- may lead to clogging that reduces the effectiveness of the ational activities. It is one of the largest freshwater wetlands scheme, requiring trained technicians to replace material. In in the tropics, involving an area of 197 ha and 12.3 m wet- Pereira Columbia, the selection of a gravel media led to fewer land plants (Trihadiningrum et al., 2007). It is hoped that instances of clogging of the filter material. To avoid limita - phytotechnologies’ incorporation of phytoremediation will tions such as this and to ensure the systems efficient removal continue to be increasingly integrated into developments, of pollutants, professional supervision over the design of wet- such as in Putrajaya, allowing continued sustainable develop- lands is crucial, highlighted by the limited control capacities ment for generations to come. of local authorities over such schemes (WSP, 2008). More generally, although phytotechnology combats many Author’s biography of the limitations of phytoremediation, its application may be Growing up on a farm in Dorset, Chloe could not fail to be constrained by the growth habit and characteristics of indi- fascinated by the natural world that surrounded her. vidual plant species, with the result that no one system is Simultaneously, it was impossible to ignore the huge effect suitable for all sites (ITRC, 2001). Thus, infiltration caps are that man was having on the landscape. These early realiza- unsuitable for areas experiencing excessive rainfall or rainfall tions influenced her BSc degree choice of Environmental so low that it cannot support plant growth (Licht et al., Science at the University of Nottingham. During her course, 2001). Wetlands may themselves become a hazard, as illus- she came to realize the complexity of the environmental trated by Keterson Marsh, USA, where a 500-ha marsh used issues involved. It became obvious that sustainable solutions to store and evaporate agricultural drainage water unknow- would only be reached if environmental goals could be ingly became contaminated with selenium that was concen- achieved while fulfilling the needs of stakeholders. For this trated in the leaves and seeds of plants, causing the death of reason, she became passionate about using our ever-increas- birds who consumed them (Horne, 2000). ing scientific knowledge to produce ecological solutions to problems which may be widely applied commercially. Chloe Conclusions hopes in future to help fulfil the potential of these technolo - gies to reduce the strain on the environment and improve the This review has considered the evolution of phytoremedia- quality of peoples’ lives. Chloe wrote this review as part of tion from initial observations of its potential to its commer- her research project in her third and final year at the University cial application today. As the fundamental properties of of Nottingham and has primary responsibility for the con- plants have essentially remained constant, this review effec- tent. She is very grateful to her co-author and supervisor tively charts the evolution of scientific thinking itself, with Colin Black, who assisted in the final write up of the paper. phytoremediation becoming simply an illustration of a much wider movement. This evolution is hinted by Lovelock (2000), who observed that the traditional bottom-up reduc- References tionist view of science is gradually progressing towards more holistic views, as seen in the transformation of phytoremedia- Alloway, J. B. (2001) Soil pollution and land contamination, in M. R. tion from the simple direct action of plants and contaminants th Chester and R. 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Journal

Bioscience Horizons – Oxford University Press

Published: Nov 4, 2014

Keywords: phytoextraction phytoremediation phytomining phytotechnologies structured wetlands infiltration caps

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