Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up

Bhupinder Dhir Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up

Bhupinder Dhir

Phytoremediation: Role of Aquatic Plants in Environmental

Clean-Up Bhupinder Dhir Department of Genetics University of Delhi South Campus New Delhi Delhi , India

ISBN 978-81-322-1306-2 ISBN 978-81-322-1307-9 (eBook) DOI 10.1007/978-81-322-1307-9 Springer New Delhi Heidelberg New York Dordrecht London

Library of Congress Control Number: 2013943842

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Springer is part of Springer Science+Business Media (www.springer.com) Preface

The depletion of water resources through environmental contamination has guided scientifi c community to develop innovative technologies for treating wastewaters. Phytoremediation using aquatic plants has emerged as an eco- friendly and cost-effective alternative. Aquatic plants irrespective free-fl oating, submerged and emergent possess immense potential for remediation of various organic and inorganic contaminants. The aquatic plants have also shown their effi ciency in removing contaminants from wastewaters when used in constructed wetlands. Since aquatic plants play a major role in phytoremediation of wastewaters, the information related to each aspect of this technique needs to be highlighted. The present book provides a detailed overview about the topic with emphasis on every aspect related to this topic.

University of Delhi, New Delhi, India Bhupinder Dhir

Acknowledgements

In compilation and completion of the major effort of this kind, I would like to acknowledge the scientiﬁ c community whose literature has been consulted extensively and that only provided the baseline for framing the whole information in form of a book. I wish to express gratitude to the Department of Science and Technology, Ministry of Science and Technology, India, for providing funding and infrastructure. I also acknowledge the website Google for providing pictures of the aquatic plants. Lastly I would like to acknowledge our publishers, Springer India, for their support.

vii

Contents

1 Introduction ...... 1 1.1 Contaminants in Aquatic Environment ...... 1 1.1.1 Physical Contaminants ...... 1 1.1.2 Chemical Contaminants ...... 1 1.1.3 Biological Contaminants ...... 4 1.2 Wastewater Treatment Methods ...... 5 1.3 Bioremediation ...... 6 1.3.1 Microbes ...... 6 1.3.2 Fungi ...... 7 1.3.3 Algae ...... 8 1.3.4 Other Materials ...... 9 1.4 Phytoremediation...... 10 1.4.1 Phytoextraction ...... 11 1.4.2 Phytostabilization ...... 13 1.4.3 Rhizoﬁ ltration (Phytoﬁ ltration) ...... 14 1.4.4 Phytovolatilization ...... 14 1.4.5 Rhizodegradation ...... 14 1.4.6 Phytodegradation (Phytotransformation) ...... 15 1.4.7 Advantages of Phytoremediation Technique ...... 15 1.5 Plant Species Used in Phytoremediation Technology ...... 15 Literature Cited ...... 19 2 Aquatic Plant Species and Removal of Contaminants ...... 21 2.1 Contaminants Removed by Aquatic Plants ...... 21 2.1.1 Inorganic Contaminants ...... 21 2.1.2 Organic Contaminants ...... 23 2.2 Major Plant Species ...... 24 2.2.1 Free-Floating Species ...... 24 2.2.2 Submerged Species ...... 32 2.2.3 Emergent Species...... 36 2.2.4 Other Plant Species ...... 40 Literature Cited ...... 41 3 Mechanism of Removal of Contaminants by Aquatic Plants ...... 51 3.1 Inorganic Contaminants ...... 51 3.1.1 Heavy Metals ...... 51 3.1.2 Radionuclides ...... 54

ix x Contents

3.1.3 Nitrogen and Phosphorus ...... 55 3.2 Organic Contaminants ...... 55 3.2.1 Halogenated Compounds ...... 59 3.2.2 Hydrocarbons ...... 61 3.2.3 Herbicides ...... 61 3.2.4 Explosives ...... 61 Literature Cited ...... 62 4 Role of Wetlands ...... 65 4.1 Constructed Wetlands (Man-Made, Artiﬁ cial or Engineered Wetlands) ...... 65 4.1.1 Composition of Wetlands ...... 66 4.1.2 Types of Wetlands ...... 67 4.1.3 Major Wetland Species ...... 68 4.1.4 Factors Affecting Functioning of Wetlands ...... 69 4.2 Mechanism of Contaminant Removal by Wetlands ...... 70 4.3 Contaminants Removed by Wetlands ...... 71 4.3.1 Inorganic Contaminants ...... 71 4.3.2 Organic Contaminants ...... 81 4.4 Limitations ...... 85 4.5 Future ...... 86 Literature Cited ...... 88 5 Future Prospects ...... 95 5.1 Limitations of Phytoremediation Technology ...... 95 5.2 Enhancement of Phytoremediation Efﬁ ciency ...... 96 5.2.1 Plant–Bacteria Symbiosis ...... 97 5.2.2 Plant–Fungi Symbiosis ...... 98 5.2.3 Biotechnological Approach ...... 98 5.3 Cost Analysis ...... 101 5.4 Conclusions and Future Developments ...... 103 Literature Cited ...... 104

About the Author...... 107

Index ...... 109 Introduction 1

Water is a resource that supports life throughout 1.1.2 Chemical Contaminants the earth. Contamination of water resulting from anthropogenic activities is a matter of concern 1.1.2.1 Organic Contaminants worldwide. Various forms of physical, chemical Biochemical oxygen demand (BOD), chemical and biological contaminants are reported in oxygen demand (COD) and total organic carbon polluted waters. Chemical pollutants mainly (TOC) are gross measures of organic content in include inorganic, organic and gaseous pollutants. wastewaters and indicate water quality. BOD is The nature of the chemical contaminant varies the amount of dissolved oxygen required by depending upon the nature of anthropogenic microbes (aerobic conditions) to break down activity and the chemicals used in various indus- organic material present in a given water sample trial processes. Discharge of municipal sewage at a certain temperature over a speciﬁ c time and industrial activities deteriorate water quality period. It is commonly expressed in milli- in urban areas. Synthetic fertilizers, herbicides, grammes of oxygen consumed per litre of sample insecticides and plant residues released from during 5 days of incubation at 20 °C. COD indi- agricultural activities change the water quality cates the mass of oxygen consumed per litre of in rural areas. solution. It is expressed in milligrammes per litre (mg L−1 ). TOC measures total carbon present in the water sample expressed in terms of content 1.1 Contaminants in Aquatic of dissolved carbon dioxide and carbonic acid Environment salts. All the three parameters determine the amount of organic pollutants found in surface Industrial, municipal and domestic wastewaters water (lakes and rivers) or wastewater. contain different types of contaminants. The com- Besides this, a large number of other organic position of wastewater depends primarily on the contaminants have been noted in wastewater organic and inorganic contaminants (Fig. 1.1 ). released from different sources. Some of the other common organic contaminants present in wastewater are listed as: 1.1.1 Physical Contaminants • Pesticides • Detergents This mainly includes colour of the wastewater, • Solvents and cleaning ﬂ uids odour and suspended solids. The level of all the • Flame retardants three parameters varies depending upon the source • Hormones and sterols of wastewater. They mainly add sludge and • Antimicrobials create anaerobic conditions. • Food additives

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 1 DOI 10.1007/978-81-322-1307-9_1, © Springer India 2013 2 1 Introduction

Color

Physical Odour

Solids

Inorganic Alkalinity, heavy metals, chlorides, sulphates, phosphates Characteristics of domestic and Chemical Organic industrial wastewaters Pesticides, surfactants, fats, oil, grease

Gaseous Hydrogen sulphide, methane, oxygen

Viruses Biological Protista

Fig. 1.1 The physical, chemical and biological characteristics of wastewater

Table 1.1 Organic contaminants reported in wastewaters (Petrović et al. 2003 ) S. no. Category Common compounds/chemicals 1 Personal care compounds DEET— N , N -diethyl-meta-toluamide Parabens—alkyl esters of p -hydroxybenzoic acid Triclosan 2 Pharmaceuticals Veterinary and human antibiotics—ciprofl oxacin, erythromycin, sulfamethoxazole, tetracycline Drugs—codeine, salbutamol, carbamazepine acetaminophen (paracetamol), ibuprofen Others—iopromide, iopamidol 3 Hormones and sterols Sex hormones—androgens, androstenedione and testosterone, and oestrogens such as oestrone, oestriol, 17 β-oestradiol, 17 α-oestradiol and progesterone 4 Surfactants Perfl uorinated sulphonates and carboxylic acids, perfl uorooctane sulphonate (PFOS) and perfl uorooctanoic acid (PFOA) 5 Solvents Trihalomethanes (THMs) and haloacetic acids (HAAs) 6 Food additives Triethyl citrate, butylated hydroxyanisole (BHA), butylated hydroxytoluene (BHT) 7 Chlorinated solvents Tetrachloroethylene (PCE), trichloroethylene (TCE), 1,1,1-trichloroethane (1,1,1-TCA), dioxin 8 Petroleum hydrocarbons Polyaromatic hydrocarbons (PAHs), methyl tertiary-butyl ether (MTBE) 9 Pesticides Chlorinated hydrocarbons (chlordane, EDB) Carbamates (aldicarb) Organophosphates (malathion) 10 Volatile organic Benzene, toluene, xylene, dichloromethane, trichloroethane, compounds (VOC) trichloroethylene 11 Endocrine disrupting Bisphenol A (BPA), oestrone, α-oestradiol and β-oestradiol 4-tert- chemicals (EDC) octylphenol (4-t-OP) and 4-n-nonylphenol (4-n-NP) 1.1 Contaminants in Aquatic Environment 3

Sources of EDCs including heptachlor, benzene, bromobenzene, chloroform, camphor, dinitrotoluene, nitrobenzene and styrene are also commonly reported in drinking and wastewaters. Point Non-Point Municipal and domestic sewage Agricultural run off Trace concentrations of endocrine-disrupting Industrial discharges Septic tanks chemicals such as oestrone, oestradiol, nonylphe- Landfill Landfill leachate nol and ethinyl oestradiol present in effl uents Farm effluents cause adverse effects in aquatic biota and hence may have an impact on human health. Exposure Fig. 1.2 Sources of endocrine-disrupting compounds that pollute the aquatic environment (From Bolong et al. 2009 ) route for both humans and animals is by inges- tion via food/drink intake which leads to bioac- Emerging or newly identifi ed contaminants cumulation and biomagnifi cation. EDCs and are a major concern for public health and safety PCPs affect reproductive potential in humans as existing conventional water treatment plants are by altering hormonal level and may prove to not designed for effective elimination of these be carcinogenic. Besides these, volatile organic unidentifi ed contaminants (Bolong et al. 2009 ) compounds (VOC) such as benzene, toluene, (Table 1.1 ). These mainly include xylenes, dichloromethane, trichloroethane (TCA) • Endocrine-disrupting chemicals (EDCs) and trichloroethylene (TCE) also contaminate (Fig. 1.2 ) water bodies through leakage from underground • Pharmaceuticals storage tanks. Most of these organic contami- • Personal care products (PCPs) nants (including chlorinated solvents, pesticides • Surfactants and hydrocarbons) are known carcinogens and • Various industrial additives neurotoxins. They cause damage to the central Organic pollutants are also referred to as nervous system, irritation of respiratory and gas- persistent organic pollutants (POPs) or xenobi- trointestinal systems and immunological, repro- otics. Pesticides are the most abundant and ductive and endocrine disorders in children. common xenobiotics present in wastewaters. These include polychlorinated dibenzodioxins 1.1.2.2 Inorganic Contaminants and dibenzofurans (often referred to as dioxins ) The presence of inorganic contaminants is very as well as polychlorinated biphenyls (PCBs), common in polluted waters. These mainly include: aldrin, toxaphene, DDT, chlordane, dieldrin, • Metals endrin, HCB, heptachlor and mirex. Concern has • Ions/nutrients arisen because these xenobiotics are extremely • Radionuclides stable and persistent, toxic to humans and other organisms, biomagnifi ed along trophic webs and Heavy Metals transported over long distances (Carvalho 2006 ). Heavy metals are elements with atomic number These xenobiotics are very resilient to biotic >20 that possess metallic properties and mainly and abiotic degradation and cause detectable include cadmium (Cd), chromium (Cr), copper harmful effects even at relatively low concentra- (Cu), mercury (Hg), lead (Pb), cobalt (Co), iron tions (Larsen 2006 ). PAHs and nitroaromatic (Fe), nickel (Ni), manganese (Mn), zinc (Zn) and compounds are of anthropogenic origin and are arsenic (As). They form a major category of produced primarily during fuel combustion and polluted waters and have been given due impor- manufacture of dyes, explosives, pesticides, tance due to their higher toxicity. Heavy metals fertilizers, etc. Most of the pesticides such as such as cadmium and lead are mainly released DDT (dichlorodiphenyltrichloroethane), aldrin, from industrial processes, industrial discharges, lindane, propiconazole and penconazole cause mining operations and acid mine drainage. hormonal imbalance and behavioural changes Alternate sources of their release are automobile and severely impact reproductive potential in exhaust, urban sewage, petrochemicals, mining humans. Aromatic and chlorinated hydrocarbons and agricultural sources such as fertilizer, fungicidal 4 1 Introduction sprays, pesticides and pharmaceuticals. Leaded rates of eutrophication. Eutrophication has been gasoline is a major source of atmospheric and ter- identifi ed as a major environmental threat in both restrial lead. freshwater and marine waters all over the globe. Ecological and anthropogenic effects of heavy Eutrophication- related water quality impairment metals are well reported (Chaney 1988 ; Wani et al. has a very substantial negative effect on water 2012). Heavy metal accumulation in living organ- quality, especially dissolved oxygen (DO) levels. isms proves toxic causing various diseases and dis- Wastewater also comprises of relatively small orders. They have tremendous affi nity for sulphur concentrations of suspended and dissolved organic and disrupt enzyme function by forming bonds and inorganic solids. with sulphur groups in enzymes. They also bind protein carboxylic (COOH) and amino (−NH2 ) Radionuclides groups. Heavy metal ions specifi cally Cd, Cr, Cu, Radionuclides are radioactive isotopes that can Pb, As and Hg bind to cell membranes, hindering occur naturally or result from man-made sources. transport processes through the cell wall. Acute Natural radiation comes from radioactive ele- toxicity cause high blood pressure, renal dysfunc- ments in the earth’s crust, groundwater and tion, neurological damage, blindness, insanity, surface water. Radionuclides such as uranium or chromosome breakage, destruction of testicular plutonium (Pt) are produced as fi ssion products and red blood cells and birth defects. Cadmium of heavy nuclei of elements or reaction of neu- in particular may replace Zn in some enzymes, trons with stable nuclei (Manahan 1994 ). They are thereby altering the stereo- structure of the enzyme formed in large quantities as waste products in and impairing its catalytic activity. Toxicological nuclear power generation. Radionuclides found effects of mercury were neurological damage, in drinking water sources are isotopes of radium including irritability, paralysis, blindness, insanity, (Ra), uranium (U) and radon (Ro), among others. chromosome breakage and birth defects. Radiation exposure can occur by ingesting, inhaling, injecting or absorbing radioactive Ions/Nutrients materials. Radionuclides have a long-term radio- Ammonia, nitrite, nitrate, chloride, sulphate, phos- logical impact due to their long half-life (e.g. phorus and cyanide (CN− ) are the major ions 30 years for 137 Cs and 2 years for 134 Cs) and present in contaminated water. Most of them are high biological availability. Half-life is the time the product of the decay of nitrogenous organic required for any given radioisotope to decay to wastes and are commonly found in groundwater one-half of its original quantity. and wastewater. The cyanide ion has a strong Industrial effl uents consist of inorganic con- affi nity for many metal ions. Cyanide is widely taminants such as heavy metals, ammonia, nitrate, used in metal cleaning, electroplating industry and nitrite, sulphate and cyanide, while oil, grease, mineral-processing operations. Ammonia is the refractory compounds, organochlorides and nitro initial product of the decay of nitrogenous organic compounds are the major organic contaminants wastes. It is a normal constituent of some sources (Nwoko 2010 ). Heavy metals, chlorides, sulphate of groundwater and is sometimes added to and nitrates are inorganic contaminants commonly drinking water to remove the taste and odour of reported in groundwater and majority of wastewa- free chlorine. Domestic, municipal and industrial ters, while pesticides, pharmaceuticals, solvents, wastewaters contain nitrogen and sulphur in high food additives, surfactants and petroleum products amounts. Sulphur is mainly present in the form are the major organic contaminants (Kolpin et al. of sulphate and other reduced forms such as 2002 ; Lin et al. 2008 ; Stuart et al. 2011 ). hydrogen sulphide, sulphides and thiosulphates. Orthophosphate is the main form of phosphorus present in wastewater streams. Nitrogen is present 1.1.3 Biological Contaminants as nitrate, nitrite or ammonium. Excessive nitrogen and phosphorus loading in wastewater is a These mainly include viruses, protists and other major threat to water quality and leads to increased pathogens such as bacteria present in wastewater. 1.2 Wastewater Treatment Methods 5

Excessive contamination in water bodies causes This is fi nally followed by disinfection diseases in humans and aquatic biota. where chlorination, ultraviolet treatment and ozonation is done to improve water quality (Fig. 1.3). 1.2 Wastewater Treatment Each of the water treatment technique is Methods effective for treating a specifi c contaminant. Heavy metals are removed mainly by alkaline Conventional technologies have been used since precipitation, ion exchange, electrochemical long for the treatment of organic and inorganic removal, fi ltration, reverse osmosis, electrodialy- contaminants present in polluted waters. The sis and adsorption. Organic pollutants such as treatment process consists of three steps: pri- polychlorinated biphenyls (PCBs) are treated by mary, secondary and tertiary. solvent extraction and thermal alkaline dechlori- Primary Treatment—The water is passed nation. Most of these technologies are based on through large tanks so that sludge can settle and physical and chemical methods that require input fl oating material such as grease and oils can rise of chemicals, which makes the technology expen- to the surface and can be skimmed off. This step sive. Moreover, they produce adverse impacts on produces a homogeneous liquid capable of being aquatic ecosystems and human health. Apart treated biologically and a sludge that can be sepa- from this, most of these techniques are practi- rately treated or processed. cally infeasible due to the range of the contami- Secondary Treatment—This removes up to nation. Over the time, all over the world 90 % of the organic matter by using biological considerable attention has been paid to select treatment processes. The microbial growth is sus- alternate methods/materials particularly biologi- pended in an aerated water mixture where the air is cal methods for wastewater treatment. Interest pumped. Aerobic bacteria and other microorgan- has been generated in the use of biosorbents for isms break down the organic matter, and most of treating industrial, municipal and domestic the organic matter is consumed by bacteria as food. wastewaters (Salt et al. 1995a ). Various biologi- Tertiary—This helps in raising the effl uent cal agents including microbes (bacteria), algae, quality by minimizing pollution. Various meth- fungi, plants and agricultural residues possess ods such as coagulation sedimentation, fi ltration potential for removing various contaminants and reverse osmosis are used. from environment and treating wastewater

Fig. 1.3 Various steps involved in treatment of wastewater using conventional method (Adapted from http://www.shef- fy6marketing.com/index.php?page ) 6 1 Introduction

Fig. 1.4 Common wastewater treatment processes (Adapted from Rawat et al. 2011 )

generated from dairies, tanneries, sugar factories, environment) capable of detoxifying a particular pulp and paper industries, palm oil mills, distill- contaminant, sometimes employing genetically eries, etc. (Fig. 1.4 ). altered microorganisms (Biobasics 2006 ). Bioremediation has been found effective in mitigating: 1.3 Bioremediation • Hydrocarbons • Halogenated organic solvents Bioremediation exploits the natural capability of • Halogenated organic compounds living organisms to clean environment. It involves • Non-chlorinated pesticides and herbicides the use of microorganisms and other biological • Nitrogen compounds materials such as algae, fungi and bacteria to • Metals (lead, mercury, chromium) detoxify or remove pollutants from the environ- • Radionuclides ment owing to their diverse metabolic capabilities (Volesky and Holan 1995 ; Matheickal et al. 1999 ; Ho et al. 2002; Malik 2004). Bioremediation aids 1.3.1 Microbes in transformation and degradation of contaminants into non-hazardous or less hazardous substances. Degradation of organic contaminants using Bioremediation technology exploits mitigation biodegradation mechanism of microbes results in processes such as biostimulation and bioaugmen- complete mineralization of organic contaminants tation. Biostimulation utilizes indigenous micro- into carbon dioxide, water and inorganic com- bial populations to remediate contaminated soils pounds, while transformation mechanism con- by adding nutrients and other substances to verts complex organic contaminants to other catalyse natural attenuation processes. Bioaug- simpler organic compounds. Biodegradation of mentation involves introduction of exogenic toxic organic pollutants such as pesticides, hydro- microorganisms (sourced from outside the soil carbons, halogenated organic compounds and 1.3 Bioremediation 7 phenolic or anilinic compounds has been facili- Microbial remediation of toxic metals occurs tated by enzymes present in microbes. Enzymes in two ways: cleave chemical bonds and assist the transfer of 1. Direct reduction by the activity of the bacte- electrons from a reduced organic substrate rial enzyme ‘metal reductase’. It is applied for (donor) to another chemical compound (accep- groundwater decontamination. This ex situ tor). Enzymes such as oxygenases or method is very expensive and has low metal oxidoreductases and laccases mediate oxidative extraction effi ciencies. coupling through polymerization, copolymeriza- 2. Indirect reduction by biologically produced tion with other substrates or binding to humic hydrogen sulphide (H2 S) by sulphate- reducing substance (Karigar and Rao 2011 ). Anaerobic bacteria to reduce and precipitate the metals. microbes are important for degrading the halo- This in situ method is environmentally sound gens and nitrosamine, reducing epoxides and and inexpensive. nitro groups. Bacteria such as Pseudomona s, The mechanism by which bioremediation of Bacillus , Neisseria , Moraxella , Trichoderma , metals occurs includes: Aerobacter , Micrococcus and Burkhol deria and 1. Biosorption and bioaccumulation Acinetobacter are able to degrade DDT, dieldrin Biosorption is sequestration of the posi- and endrin. Anabaena (a cyanobacterium), tively charged heavy metal ions (cations) to Pseudomonas spinosa , Pseudomonas aeruginosa the negatively charged microbial cell mem- and Burkholderia can degrade endosulfan. branes and polysaccharides secreted in most Microorganisms employ a variety of mecha- of the bacteria on the outer surfaces through nisms to resist and cope with toxic metals. slime and capsule formation. The metals are Oscillatoria spp., Chlorella vulgaris and transported into the cell cytoplasm through Chlamydomonas spp., Arthrobacter , Agrobacter , the cell membrane with the aid of transporter Enterobacter and Pseudomonas aeruginosa are proteins. some metal-reducing microbes. The principal 2. Immobilization mechanism of resistance of inorganic metals Metal ions get fi xed to iron (Fe) oxides and by microbes are oxidation, reduction, methylation, into organic colloids inside the microbial cells demethylation, enzymatic reduction, metal– become immobilized. This is achieved by organic complexion, metal ligand degradation, enzymatic reduction by microbes. intracellular and extracellular metal sequestra- 3. Solubilization tion, metal effl ux pumps, exclusion by permea- Metal-reducing bacteria enzymatically bility barrier and production of metal chelators reduce and also solubilize oxide minerals. such as metallothioneins and biosurfactants. Microorganisms do not biodegrade inorganic metals, but transform their oxidation state. 1.3.2 Fungi Transformation of oxidation states of toxic metals increases their bioavailability in the rhizo- Penicillium , Aspergillus wentii , Aspergillus niger sphere (root zone), thus facilitating their Rhizopus oryzae , Mucor , Saccharomyces , Pha- absorption and removal. Generally, microbial nerochaete chrysosporium (white rot fungi), transformations and detoxifi cations of metals Trametes versicolor , Pleurotus ostreatus and occur by either redox conversions (reduction) of Pleurotus sajor - caju biosorb metals and radionu- inorganic forms or conversions from inorganic to clides (Bishnoi and Garima 2005 ). Biosorption organic forms and vice versa. Reduction of met- of metal ions on cell surface occurs by ion als can occur through dissimilatory metal reduc- exchange and complexation with functional tion, where microbes utilize metals as terminal groups such as carboxylate, hydroxyl, amines, electron acceptor for anaerobic respiration. Till amide, phosphate and sulphydryl. Extracellular date As, Cr, Hg, U and Se have been detoxifi ed enzymes such as oxidoreductases, laccases, ligni- by microbial reduction. nases and peroxidases present in fungus assist 8 1 Introduction

Table 1.2 Bacteria capable of destroying hazardous wastes and chemicals by biodegradation Organisms Chemicals degraded Bacteria Flavobacterium spp. Organophosphates Cunniughamella elegans and Candida tropicalis PCBs (polychlorinated biphenyls) and PAHs (polycyclic aromatic hydrocarbons) Alcaligenes spp. and Pseudomonas spp. PCBs, halogenated hydrocarbons, alkylbenzene sulphonates, PCBs, organophosphates, benzene, anthracene, phenolic compounds, 2,4-D, DDT and 2,4,5-trichlorophenoxyacetic acid etc Actinomycetes Raw rubber Nocardia tartaricans Chemical detergents (ethylbenzene) Arthrobacter and Bacillus Endrin Closteridium Lindane Trichoderma and Pseudomonas Malathion Fungi Phanerochaete chrysosporium Halocarbons such as lindane and pentachlorophenol P . sordida and Trametes hirsuta DDT, DDE, PCBs, 4,5,6-trichlorophenol, 2,4,6-trichlorophenol, dichlorphenol and chlordane Zylerion xylestrix Pesticides/herbicides (aldrin, dieldrin, parathion and malathion) Yeast (Saccharomyces ) DDT Mucor Dieldrin degradation of xenobiotic compounds including Ankistr odesmus and Scenedesmus have been lignocellulosic materials, phenols PAHs, PCBs, successfully used for the treatment of olive oil, mill, nitroaromatics, pesticides, herbicides and dyes paper industry and domestic wastewater. Removal (Magan et al. 2010 ). Fungal peroxidases and of contaminants occurs by bioaccumulation and dioxygenases are involved in biodegradation of biodegradation. The unicellular green algae pentachlorophenol. White rot fungi in particular Chlorella fusca var. vacuolata and Chlamydo- produce lignin-degrading enzymes that catalyse monas reinhardtii are able to bioaccumulate, oxidation of xenobiotics such as endosulfan in biotransform and biodegrade the herbicide addition to their ability to degrade lignin. metfl uorazon and prometryne and remove Aspergillus fl avus , Fusarium oxysporum , Mucor nutrients such as nitrogen and phosphorus. aternans , P . chrysosporium , Trichoderma Ankistrodesmus and Scenedesmus species have viride, etc. degrade DDT. Biodegradation of also shown potential for biotransforming organic pesticides is regulated by environmental factors compounds such as naphthalene. including pH, temperature, nutrient supply and Algal species such as Chlorella , Anabaena oxygen availability. Biodegradation occurs via inaequalis , Westiellopsis prolifi ca , Stigeoclonium two strategies: (1) the use of the target com- tenue and Synechococcus sp. tolerate heavy pound as a carbon source and (2) enzymatic metals. Several species of Chlorella , Anabaena transformation of the target compound (co- and marine algae have been used for the removal metabolism) (Table 1.2 ). of heavy metals. Metals are taken up by algae through adsorption. At fi rst, the metal ions are quickly adsorbed over the cell surface in a few 1.3.3 Algae seconds or minutes; this process is called physical adsorption. Then, these ions are trans- Algae acts as indicators of water pollution ported slowly into the cytoplasm in a process and play a role in treating wastewater. Algae called chemisorption. Polyphosphate bodies in such as Chlamydomonas reinhardtii , Chlorella , algae enable freshwater unicellular algae to 1.3 Bioremediation 9

Algae Compounds

Petroleum compounds Selanastrum capricornatum Cyanobacteria(Blue-green algae) Benzene, toluene, naphthalene, pyrene, Microcystis aeruginosa acrylonitrile, Dibenzanthraceae, fluoroanthene, petroleum hydrocarbons

Chlamydomona sp. Pesticides Chlorella sp. DDT, parathion, phenol, benzene, Chlorococcum sp. toluene, chlorobenzene, Cylindrotheca sp 1,2-dichlorobenzene, nitrobenzene Dunaliella sp. naphthalene, 2,6-dinitrotoluene, Euglena gracilis phenanthrene, di-nbutylphthalate, Scenedesmus obliquus Toxaphene, methoxychlor Selenastrum capricornutum

Fig. 1.5 Degradation of organic compounds by algae

store other nutrients. Several researchers have treatment. Agro residues and biomaterials such as established that metals such as Ti, Pb, Mg, Zn, leaf powder, straw and bran, fruit residues, ﬁ bres Cd, Sr, Co, Hg, Ni and Cu are sequestered in obtained from crop plants, fruit plants and tree spe- polyphosphate bodies in green algae. These bodies cies have been evaluated with an aim of developing perform two different functions in algae: provide low-cost wastewater treatment technology (Ho and a ‘storage pool’ for metals and act as a ‘detoxiﬁ - Ofomaja 2006 ; Ofomaja and Ho 2007 ; Amuda cation mechanism’. Microcystis microalgae are et al. 2007; Kahraman et al. 2008; Schiewer and capable to synthesize peptides and metallothio- Patil 2008 ). These materials have been found effec- neins, mainly the post-transcriptionally synthesized tive in removing heavy metals; inorganic ions such class III metallothioneins or phytochelatins, which as nitrate, ammonia and phosphate; and organic effectively bind to heavy metal (Dwivedi 2012 ). compounds including dyes and phenol (Sun and Among them, microalgae have proved to possess Xu 1997 ; Abdelwahab et al. 2005 ; Ho et al. 2005 ; high metal-binding capacities due to the presence Eberhardt and Min 2008 ; Mohd Din et al. 2009 ; of polysaccharides, proteins or lipid on the Liu et al. 2010 ). Removal of contaminants occurs surface of their cell walls containing some func- by adsorption, chelation and ion exchange (Gardea- tional groups such as amino, hydroxyl, carboxyl Torresday et al. 1999). These materials are com- and sulphate, which can act as binding sites posed of lignin, cellulose, hemicellulose, pectin for metals. Marine algae are capable of bio- and tannins that possess functional groups such as sorbing radionuclide such as radium, thorium alcohols, hydroxyls, aldehydes, ketones, carboxyl- and uranium (Priyadarshani et al. 2011 ). ates and phenols that contribute to native ion Biosorption of uranium by Cystoseira indica , a exchange capacity (Abia et al. 2002 ). High adsorp- brown alga, has also been reported (Fig. 1.5 ). tion capacity, availability in bulk and low economic value are advantages associated with the use of agro residues. 1.3.4 Other Materials Terrestrial as well as aquatic plant species show ability to remove/transform/degrade con- Agricultural products/by-products are natural sorbent taminants. Crop plants, tree species, weeds and materials that have also shown the capacity to remove other wild plants with their natural ability in contaminants from wastewater. They can serve as a removing various contaminants from the envi- replacement of costly methods for wastewater ronment have been demonstrated. 10 1 Introduction

husk of Cicer arietinum, Vigna mungo, Oryza sativa, sugarcane Crop residues bagasse, wheat straw, bran and shell, rice husk

sugar-beet pulp, apple pomace, citrus peels, coconut copra Fruit residues meal, coconut shell, orange mesocarp, carrot residues, apricot seeds, pomegranate, cocoa shells, apple pomace

spruce, coconut coir, kenaf bast, kenaf core, cotton, Oil palm Fibers fibers Heavy metals, neem (Azadirachta indica) leaf powder, Petiolar felt sheath of dyes, palm, Boston ivy leaves and stems, southern magnolia leaves, nutrients Plant/tree sawdust, poplar leaves, sunflower stalks, flower Picea abies residues (Norway spruce), aspen wood fibers, P. jezoensis (Yezo spruce) bark

almond shell, hull (Prunus dulcis), groundnut shell, Others Tamarindus indica seed, walnut shell (Juglans regia), hazelnut shell (Corylus avellana),Moringa (Moringa oleifera) seed powder, Jatropha seed coat

Fig. 1.6 Various agricultural residues used for removing contaminants from wastewater

Bioremediation techniques, although requiring for treating both organic and inorganic contami- more time, usually require less capital (~10–50 % nants present in water and soil and hence can be cheaper) than the physical and chemical treat- an affordable technological solution for waste- ment methods. Bioremediation has been listed water treatment. The high purifi cation activity among top ten technologies because of its poten- of the plants is due to a rapid growth in polluted tial for sustainable mitigation of environmental wastewater and capacity to remove contami- pollution and cost effectiveness. In the era of bio- nants (Miretzky et al. 2004 ). Plants possess remediation, vegetation/plants as a biological effi cient capacity for removing/treating variety resource with immense capacity for removing of contaminants- metals, pesticides, chlorinated variable contaminants from various components solvents, explosives, crude oil, polycyclic aro- of ecosystem have been studied. Plants remove or matic hydrocarbons, polychlorinated biphenyls, degrade selected contaminants present in soil, landfi ll leachates, munitions and radionuclides sludge, sediment, groundwater, surface water and through processes such as extraction, degrada- wastewater by utilizing their metabolic and tion, or including military sites, agricultural hydraulic processes, thereby improving the envi- fi elds, industrial units, mine tailings, and sew- ronment quality that is termed as ‘phytoremedia- age and municipal wastewater treatment tion’ (Fig. 1.6 ). plants. Bioremediation technologies, including phytoremediation, have been estimated to be 4–1,000 times cheaper, on a per volume basis, 1.4 Phytoremediation than current non-biological technologies (Sadowsky 1999 ). Phytoremediation has been Plant root systems together with the transloca- studied extensively in research and small-scale tion, bioaccumulation and contaminant degra- demonstrations, but full-scale applications dation abilities aid the technique. Over the time, are currently limited to a small number of proj- green technology became a promising alternate ects (Cunningham and Ow 1996 ). 1.4 Phytoremediation 11

The uptake of contaminants by plants is • Plant biomass—The high-biomass-producing affected by several factors. Major factors include: plants possess higher contaminant removal • Plant species—The physical characteristics of potential. plants play an important role in the uptake/ Phytoremediation technology can treat both removal of contaminants. Genetic adaptations organic and inorganic contaminants, though uptake and biological processes including metabolic mechanisms in plants vary for each contaminant and absorption capabilities transport systems (Barceló and Poschenrieder 2003 ). Treatment of help in uptake of nutrients or contaminants organic contaminants mainly involves phytostabi- selectively from the growth matrix (soil or lization, rhizodegradation, rhizofi ltration, phyto- water). Higher biomass production and spe- degradation and phytovolatilization mechanisms, cies with higher adaptability to climatic and while phytostabilization, rhizofi ltration, phytoac- soil conditions are a necessary requirement cumulation and phytovolatilization mechanisms for good phytoremediation capacity. Plant are involved in the treatment of inorganic contami- processes and associated rhizosphere microbes nants (Fig. 1.7 ; Table 1.3 ). help in degradation/detoxifi cation/transfor- A number of different methods lead to mation of contaminants. Selection of the contaminant degradation, removal (through plant species whether annuals or perennials, accumulation or dissipation) or immobilization: monoculture or deciduous is an important 1. Degradation (destruction or alteration of consideration. The seeds or plants should be organic contaminants)—rhizodegradation and from, or adapted to, the climate of the phy- phytodegradation toremediation site. Therefore, the selection of 2. Accumulation (removal of organic and/or plant variety is critical to ensure superior and metal contaminants)—phytoextraction and effective remediation. For metal remediation, rhizofi ltration identifi cation and selection of suitable hyper- 3. Dissipation (removal of organic and/or inor- accumulator plant species is required (Schnoor ganic contaminants into the atmosphere)— et al. 1995 ). phytovolatilization • Physical properties—Physicochemical param- 4. Immobilization (containment of organic and/or eters such as pH, organic matter, redox poten- inorganic contaminants)—phytostabilization tial, contaminant concentration and the mineral content of the soil and water affect the removal/degradation of the contaminant. 1.4.1 Phytoextraction • Root zone—Root length and root diameter affect contaminant uptake and degradation. It is defi ned as uptake/absorption and translocation Degradation of contaminants in the soil is of contaminants by plant roots into the above- facilitated by plant enzymes and root exu- ground portions of the plants (shoots) that can be dates. Plant roots exude organic acids such harvested. Plant species absorb and hyperaccu- as citrate and oxalate that affect the bio- mulate metal contaminants and/or excess nutrients availability of metals. The type, amount and in harvestable root and shoot tissue. This process effectiveness of exudates and enzymes pro- is applicable for metals (Ag, Cd, Co, Cr, Cu, Hg, duced by a plant’s root vary between species Mn, Mo, Ni, Pb, Zn), metalloids (As, Se), radio- and even within subspecies or varieties of nuclides (90 Sr, 137Cs, 234U, 238U), non-metals one species. (B, Mg) and organic contaminants present in soils, • Chelating agent—Chelating agents such as sediments and sludges (Brooks 1998a ). It is EDTA and micronutrients increase the bio- also referred to as phytoaccumulation, phytoab- availability of contaminants especially heavy sorption, phytosequestration, phytomining or metals and stimulate the heavy metal-uptake biomining. Thompson et al. (1998 ) reported phy- capacity of the plant so that remediation is toaccumulation of organic contaminants, mainly faster. explosive hexahydro-1,3,5-trinitro- 1,3,5-triazine 12 1 Introduction

Phytoaccumulation

Phytovolatilization Phytodegradation

Phytoextraction Phytostimulation

Phytostabilization Rhizodegradation

Rhizofiltration

Fig. 1.7 Phytoremediation processes

Table 1.3 Phytoremediation processes Process Description Media Contaminants Plants Rhizodegradation/ Microbial degradation Soil, sediments, Organic—aromatic, Grasses, alfalfa, phytodegradation in the rhizosphere sludges aliphatic and hybrid poplar, stimulated by plants petroleum Brassica , Typha , hydrocarbons, Jatropha , Cassia chlorinated solvents, TNT, pesticides Phytostabilization Stabilization of Soil, sediments, Inorganic—metals (As, Sunfl ower, contaminants by sludges Cd, Cr, Cu, Pb, Zn) Chenopodium binding/complexation Phytoextraction Uptake of Soil, sediments, Inorganic—metals (Cr, Alyssum , Brassica contaminants into sludges Cu, Ni, Zn, Cd, Ag), Thlaspi , sunfl ower roots by accumulation radionuclides or harvestable shoots Rhizofi ltration Removal of Groundwater, Inorganic—metal, Eichhornia , Lemna contaminant by surface water, radionuclides (137 Cs, plant roots wastewater 230 Pb, 238 U) Phytovolatilization Volatilization of Soil, sediments Organic/inorganic (Se, Poplar , Phragmites , contaminant by leaves Hg, As) Scirpus

(RDX), in an unaltered form in the leaves of concentration noted in these plants are about hybrid poplar from a hydroponic solution. 10–100-fold higher than the levels noted in ‘ordi- nary’ non-hyperaccumulator plants (Erakhrumen 1.4.1.1 Hyperaccumulators 2007 ; Wani et al. 2012 ). The minimum concentra- Plants that possess the capacity to accumulate tion of metal a plant needs to contain to be termed high quantities of metals than required for plant a hyperaccumulator varies for each metal (Reeves growth are termed as ‘hyperaccumulators’. The and Brooks 1983 ; Baker and Brooks 1989 ). They 1.4 Phytoremediation 13

Table 1.4 Range of elemental concentrations in non- hyperaccumulator and hyperaccumulator plants (Reeves 2003 ) Element Normal range (mg g − 1 ) Element limit (mg g − 1 ) Hyperaccumulator species As 0.01–5 1,000 Pteris vittata Cd 0.03–20 100 Eichhornia crassipes , Thlaspi caerulescens Co 0.05–50 1,000 Alyssum sp. Cu 1–100 1,000 Elodea nuttallii Mn 5–2,000 10,000 Alyssum sp. Phytolacca acinosa Ni 0.2–100 1,000 Berkheya coddii , Alyssum bertolonii Cr 0.05–30 1,000 Spirodela polyrhiza , Dicoma niccolifera Sutera fodina Pb 0.5–30 1,000 Thlaspi rotundifolium Minuartia verna Brassica sp. Sesbania drummondii Se 0.01–10 100 Astragalus bisulcatus Stanleya pinnata Zn 0–0.1 10,000 Thlaspi caerulescens Eichhornia crassipes

are defi ned as plants that complete their life cycle adsorption onto roots or precipitation within with foliar metal concentrations exceeding (mg the root zone preventing their migration in soil. kg−1 dry weight, DW) Cd > 100, Ni and Cu > 1,000 The plant root exudates stabilize, demobilize and Zn and Mn > 10,000 (Table 1.4 ). This is phys- and bind the contaminants in the soil matrix, iologically possible because they possess high thereby reducing their bioavailability. This pro- tolerance capacity (Brooks 1998a , b ). Most of the cess is suitable for organic contaminants and metal taken up by them is exported to shoots, metals present in soils, sediments and sludges. while a lower proportion of them are stored in Contaminants are adsorbed onto roots or bind to root vacuoles. Some of the most studied hyperac- humic (organic) matter through the process of cumulator plant species include Thlaspi , Pteris humifi cation. Phytostabilization of organic con- vittata, and Brassica species (Brooks 1998a , b). taminants or metabolic by-products can be These plants can accumulate metals in concentra- achieved by attaching to plant components such tions 100,000 times greater than in the associated as lignin. This is referred to as ‘phytolignifi ca- water. Maximum number of hyperaccumulators tion’ (Cunningham et al. 1995 ). Phytostabilization have been reported from families Brassicaceae, of metals is generally intended to occur in the Lamiaceae, Scrophulariaceae, Cyperaceae, soil, whereas phytostabilization of organic Poaceae, Apocynaceae, Euphorbiaceae, Flacourt contaminants through phytolignifi cation occurs iaceae, Fabaceae and Violaceae. aboveground. Metals within the root zone can be stabilized by changing from a soluble to an insoluble oxidation state, through root-mediated 1.4.2 Phytostabilization precipitation. Plant root exudates and microbes present in root zone alter the soil pH by the produc-

It is defi ned as the use of plants to immobilize the tion of CO2 , possibly changing metal solubility contaminants in the soil and groundwater through and mobility, thus impacting the dissociation absorption and accumulation in plant tissues, of organic compounds. This technique does not 14 1 Introduction require disposal of hazardous materials or biomass. molecule contaminants. The degradation product Moreover, ecosystem restoration is enhanced by or modifi ed volatile form is less toxic than the the vegetation. The only limitation is long-term main contaminant. Examples include the reduc- maintenance of the vegetation. tion of highly toxic Hg species to less toxic elemental Hg or transformation of toxic Se (as selenate) to the less toxic dimethyl selenide gas. 1.4.3 Rhizofi ltration Genetically modifi ed tobacco (Nicotiana taba- (Phytofi ltration) cum ) and Arabidopsis thaliana contain a gene for mercuric reductase that convert ionic mer- It is the removal of contaminants in surface water cury (Hg(II)) to the less toxic metallic mercury by plant roots. It involves adsorption or precipita- (Hg(0)) and volatilize it (Meagher 2000 ). tion onto plant roots or absorption followed by sequestration in the roots. This process is applicable for removal of metals (Pb, Cd, Cu, Fe, Ni, 1.4.5 Rhizodegradation Mn, Zn, Cr), excess nutrients and radionuclide (90 Sr, 137 Cs, 238 U, 236 U) present in groundwater, It is defi ned as the breakdown of contaminants in surface water and wastewater (Dushenkov et al. the soil through microbial activity localized in 1995 , 1997a , b). It is generally applicable for the root zone. This process uses microorganisms treating large volumes of water with low contam- to consume and digest organic substances for nutri- inant concentrations (ppb). It can be conducted tion and energy. Natural substances/exudates in situ or ex situ to remediate contaminated sur- released by plant roots include sugars, alcohols, face water bodies. Parameters such as pH, fl ow amino acids, organic acids, fatty acids, sterols, rate and contaminant concentration can alter the growth factors, nucleotides and fl avanones; contain effi ciency of this process. Applications of rhizo- organic carbon that provides food for soil microfi ltration are currently at the pilot-scale stage. organisms; and establish a dense root mass that Phytotech tested a pilot-scale rhizofi ltration system takes up large quantities of water. Organic con- in a greenhouse at the Department of Energy taminants in soil can often be broken down into uranium-processing facility in Ashtabula, Ohio, daughter products or completely mineralized to and engineered ex situ system used sunfl owers to inorganic products such as carbon dioxide and remove uranium from contaminated groundwater water by naturally occurring bacteria, fungi and and/or process water (Dushenkov et al. 1997a , b ). actinomycetes. Plant roots increase the size and Proper disposal of the contaminated plant biomass variety of microbial populations in the soil could be a limitation. surrounding the roots (the rhizosphere) or in mycorrhizae (associations of fungi and plant roots). The increased microbial populations and 1.4.4 Phytovolatilization activity in the rhizosphere result in increased contaminant biodegradation in the soil, and It is defi ned as the plant’s ability to absorb, degradation of the exudates can stimulate co- metabolize and subsequently volatilize the con- metabolism of contaminants in the rhizosphere. taminant into the atmosphere. Growing trees Plant root exudates also alter geochemical condi- and other plants take up water along with the tions in the soil, such as water content, aeration, contaminants, pass them through the plants structure, temperature and pH, which may result leaves and volatilize into the atmosphere at in changes in the transport of inorganic contaminants comparatively low concentrations. This process creating more favourable environments for soil is used for removing metal contaminants pres- microorganisms. Perhaps the most serious imped- ent in groundwater, soils, sediments and sludge iment to successful rhizodegradation is the depth medium. This process is applicable for complex of the root zone. A wide range of organic con- organic molecules that are degraded into simpler taminants such as petroleum hydrocarbons, PAHs, 1.5 Plant Species Used in Phytoremediation Technology 15 pesticides, chlorinated solvents, PCP, polychlori- minimal environmental disruption. This is because nated biphenyls (PCBs), benzene, toluene, it possesses certain advantages such as: o-xylene and surfactants can be removed by this • Capacity in reducing a wide range of contami- technique (Donnelly et al. 1994 ; Gilbert and nants both organic and inorganic. Crowley 1997 ). • Cost-effective technology as it does not require expensive biosorbent materials and highly specialized personnel and equipment. 1.4.6 Phytodegradation It is cost-effective for large volumes of water (Phytotransformation) having low concentrations of contaminants and for large areas having low to moderately It is defi ned as the metabolization and degradation contaminated surface soils. of contaminants within the plant or the degrada- • Can be applied in situ to remediate shallow tion of contaminants in the soil, sediments, slud- soil, groundwater and surface water bodies. ges, groundwater or surface water by enzymes • Does not have destructive impact on environment produced and released by the plant. Organic com- and benefi ts the soil, leaving an improved, pounds such as munitions (trinitrotoluene), chlori- functional soil ecosystem at costs estimated nated solvents, herbicides, insecticides and at approximately one-tenth of those currently inorganic nutrients are reported to be removed by adopted technologies. this technique (Burken and Schnoor 1997 ; • Can be used in much larger-scale cleanup Thompson et al. 1998; Campos et al. 2008 ). Plant- operations. produced enzymes metabolize contaminants that • Organic pollutants may be degraded to CO2 may be released into the rhizosphere. Plant-formed and H 2 O removing environmental toxicity. enzymes found in plant sediments and soils • Can decontaminate heavy metal-polluted soils include dehalogenase, nitroreductase, peroxi- and biomass produced during the phytoreme- dase, laccase and nitrilase (Schnoor et al. 1995 ). diation process could be economically Nitroreductase enzyme present in Myriophyllum valorized in the form of bioenergy. The use of aquaticum degrades TNT concentrations (Schnoor metal-accumulating bioenergy crops might be et al. 1995 ). Hybrid poplar trees metabolized suitable for this purpose. TNT to 4-amino-2,6-dinitrotoluene (4-ADNT), 2-amino-4,6-dinitrotoluene (2-ADNT) and other unidentifi ed compounds in laboratory hydroponic 1.5 Plant Species Used and soil experiments (Thompson et al. 1998 ). in Phytoremediation Pilot-scale fi eld demonstration studies of phyto- Technology degradation have been conducted for a number of sites, primarily army ammunition plants Terrestrial and aquatic plant species have been (AAPs) contaminated with munitions waste, exploited for phytoremediation. Terrestrial spe- including the Iowa AAP, Volunteer AAP and cies have been found effective for phytoremedia- Milan AAP, and emergent aquatic plants have tion as they possess larger root systems which shown potential to decrease TNT concentrations. facilitate higher uptake of contaminants. Trees and grass species are commonly used for phytoremediation. Alfalfa has been used widely for 1.4.7 Advantages its deep rooting and root zone metabolic activity. of Phytoremediation Poplar (or hybrid poplar) and cottonwood Technique ( Populus deltoides) trees, Indian mustard Brassica juncea , sunfl ower (Helianthus annuus ), Over the last few years, phytoremediation emerged Thlaspi sp. including T . caerulescens and T . rotun- as a publicly acceptable, aesthetically pleasing difolium have been explored because of the and solar-energy-driven cleanup technology with characteristics such as high biomass production 16 1 Introduction

Fig. 1.8 Some of the terrestrial species used in phytoremediation: ( a ) Thlaspi , ( b) Pteris, ( c) Helianthus and ( d ) Populus and fast growth (EPA 1998 ; Schnoor 2000 ). 1. The vetiver grass (Vetiveria zizanioides ) Several fast-growing tree plantations have been The plant was able to treat (biological) established and are under active study for their 16,000 tonnes of soils contaminated with potential use in wastewater cleanup in land dis- polyaromatic hydrocarbons (PAHs) at the charge systems. Some grasses such as ryegrass, Scott Lumber Company site in Missouri, prairie grasses and fescues have been investi- USA. The PAH concentration was effectively gated for rhizodegradation and phytostabilization reduced by 70 %. due to their widespread growth and their exten- 2. The brake fern (Pteris vittata ) sive root systems. Efﬁ cacy of phytoremediation The Edenspace System Corporation in the varies according to varieties, cultivars or genotypes USA used the Chinese brake fern, and it and type of pollutant (Dipu et al. 2011 ). showed potential to treat 1.5-acre site con- Each plant species depicts a variation in its abil- taminated with arsenic (As) in New Jersey, ity to remove contaminants from the environment. North Carolina. The fern phytoextracted Plants such as Pteris vittata , Sutera fodina , more than 200-fold of arsenic (As) in the Alyssum and Thlaspi rotundifolium possess the above-ground part. capacity to remove heavy metals such as As, Cr, 3. Hybrid poplar (Populus × canadensis ) Ni, Zn and Cd, while Zea mays , Setaria faberi , Ecolotree Inc. used the hybrid poplar trees Solanum melongena , Spinacia oleracea , Raphanus to phytoremediate soil and groundwater con- sativus , Ocimum basilicum and Oryza sativa have tamination with petroleum-related organics, shown the ability to transform and bioaccumulate PAHs and chlorinated organics released herbicides and pesticides like DDT and endosul- by accidental spills in 2000 in Milwaukee, fan. Hordeum vulgare and Conyza canadensis Wisconsin, USA. The poplar trees were buried have shown sequestration of herbicide metolachlor up to 10 ft below the surface, and a subsurface and glyphosate in vacuoles (Fig. 1.8 ). aeration system was provided to encourage Some plants that have shown high potential deep rooting into groundwater. Ecolotree Inc. used for phytoremediation have been listed below: the hybrid poplar to treat soil contaminated 1.5 Plant Species Used in Phytoremediation Technology 17

with chemical fertilizer and pesticides in at Aberdeen, Maryland. The sunfl ower plants Illinois, USA, in 1999. Some 440 trees of bioaccumulated uranium at the rate of 764 mg about 12–18 ft tall bare root poplar were kg−1 –1,669 mg kg−1 of soil. planted into 6-ft-deep trenches. 5. Indian mustard (Brassica juncea ) The Occidental Petroleum Corporation, The Edenspace System Corporation, USA, LA, and the University of Washington, USA, used the Indian mustard plant to treat the used hybrid polar to treat several sites in the radionuclide strontium (Sr89/90)-contaminated USA contaminated with ‘trichloroethanol’. soil at Fort Greely in Alaska, USA. The plants Hybrid polar trees were successfully used by bioaccumulated more than 10–15-fold of stron- other commercial companies like Phyto- tium (Sr89/90) higher than in soil. They also kinetics Inc. in the USA to treat groundwater used the Indian mustard with sunfl ower to treat contaminated with chlorinated volatile organics various sites in the USA contaminated with including dichlorobenzidine at several super- heavy metals. They accumulated more than fund sites. Technical University of Denmark 3.5 % of heavy metals of their dry weight. They used poplar trees to phytoremediate soils also used the Indian mustard to remove contaminated by gasoline and diesel com- caesium-137 (Cs137) from the contaminated pounds at an old gas fi lling station at Axelved, pond waters after the Chernobyl Nuclear Power Denmark, and cyanide, PAHs, oil and BTEX Plant disaster in Ukraine in 1986. (benzene, toluene, ethylbenzene and xylene) The Brookhaven National Lab, New Jersey, contaminated soil at a former municipal gas USA, used Indian mustard to remove radionu- work site in Denmark. The Polish Academy clides cesium-137 (Cs137 ) and strontium-90 of Sciences used the poplar trees to remove (Sr90) by phytoextraction from contaminated pesticides stored in bunkers at a resort in soil. The Phytotech, Florida, USA, used the Niedzwiada, Poland. Indian mustard plant to remediate lead (Pb)- 4. Sunfl ower (Helianthus annuus ) and cadmium (Cd)-contaminated soil at the Sunfl ower plants has been used to treat Czechowice Oil Refi nery, Katowice, in lead-contaminated soil with lead (Pb) ranging Poland. Indian mustard plant was used with from 75- to 3,450-mg kg−1 soil at its Detroit sunfl ower (Helianthus annuus ) to phytoreme- Forge Site in 1998. In a single season of crop diate the lead (Pb)-contaminated soil at an growth, the lead contents in the soil were industrial facility in Connecticut, USA. brought down to 900 mg kg−1 of soil, and sub- Literature demonstrates many success stories sequently it was removed completely after related to removal of variable contaminants at successive crop growth. The total cost of phy- various sites across the world (Table 1.5 ). toremediation treatment by sunfl ower was US Realizing the potential of terrestrial species, $ 50.00 per cubic yard, which saved more than aquatic plant species have been explored and US $ 1.1 million compared to the estimated studied extensively for their phytoremediation cost of physicochemical treatment by soil capacity. A number of aquatic plant species and excavation and disposal in landfi lls. their associated microorganisms have been used Sunfl ower and the Indian mustard plant for more than a decade in constructed wetlands (Brassica juncea) were used to phytoremedi- for municipal and industrial wastewater treat- ate the lead (Pb)-contaminated soil at an ment. The aquatic plant biomass represents an industrial facility in Connecticut, USA. The abundantly available biological material. The Edenspace System Corporation in the USA features such as easily cultivation, high biomass used the sunfl ower and the Indian mustard to production, faster growth rate, surplus avail- treat various sites in the USA contaminated ability and high tolerance to survive adverse with heavy metals. The company also used this environmental conditions together with higher plant to remediate uranium (U)-contaminated bioaccumulation potential establish them as soils (47 mg kg−1 of soil) at the US Army Sites potential agents for phytotechnology. Aquatic 18 1 Introduction

Table 1.5 Sites demonstrating phytoremediation of various contaminants Location Application Pollutant Medium Plants Edgewood, MD Phytovolatilization Chlorinated solvents Groundwater Hybrid poplar Rhizofi ltration Hydraulic control Forth Worth, TX Phytodegradation Chlorinated solvents Groundwater Eastern cottonwood Phytovolatilization Rhizodegradation Hydraulic control Ogden, UT Phytoextraction Petroleum Soil Alfalfa, poplar Rhizodegradation Hydrocarbons Groundwater Juniper, fescue Portsmouth, VA Phytodegradation Petroleum Soil Grasses Rhizodegradation Clover Trenton, NJ Phytoextraction Heavy metals Soil Hybrid poplar Radionuclides Grasses Anderson, ST Phytostabilization Heavy metals Soil Hybrid poplar, grasses Ashtabula, OH Rhizofi ltration Radionuclides Groundwater Sunfl ower Milan, TN Phytodegradation Explosives Groundwater Duckweed, parrot feather Amana, IA Phytodegradation Nitrates Groundwater Hybrid poplar Upton, NY Phytoextraction Radionuclides Soil Indian mustard, cabbage Chernobyl, Ukraine Rhizofi ltration Radionuclides Groundwater Sunfl owers Source : Adapted from EPA (1998 ) and the website ( http://arabidopsis.info/students/dom/mainpage.html ) plants also referred to as aquatic macrophytes (b) Floating attached—Plants that have leaves consist of/include assemblage of diverse taxo- fl oating on the surface, stems beneath the nomic groups including pteridophytes (ferns) and surface and roots anchoring to the substrate. bryophytes (mosses, hornworts and liverworts) 2 . Submerged plant species —They include spe- and angiosperms (fl owering plants). They domi- cies where the entire plant is below the surface nate in wetlands, shallow lakes, ponds, marshes, of the water. Some of well-explored species in streams and lagoons. They play key functions in this category include Potamogeton , Cerato- biochemical cycles, through organic carbon phyllum and Myriophyllum production, phosphorous, mobilization and the 3 . Emergent plant species —They include spe- transfer of other trace elements and act as carbon cies whose stems and leaves are found above sinks. They directly infl uence the hydrology and the water, while the roots grow underwater. sediment dynamics of freshwater ecosystems Some common species in this category are through their effects on water fl ow. Typha , Elodea , Phragmites and Scirpus . Macrophytes are broadly classifi ed into three The aquatic and wetland plant species—in types depending upon their habit of growth: particular, free-fl oating, submerged (rooted) and 1 . Free - fl oating plant species —They are further semiaquatic/emergent (rooted)—gained impor- classifi ed as: tance worldwide as they depict exorbitant effi - (a) Floating unattached—Plants that fl oat on ciency to remove contaminants from wastewaters, the surface of water and roots/submerged though the degree of potential for removal varies leaves hang free in the water, i.e. they are from species to species. Aquatic macrophytes not anchored to the bottom. Some of the possess immense potential for removal/degrada- well-studied species in this category are tion of variety of contaminants, including heavy Lemna , Eichhornia , Pistia , Salvinia , metals, inorganic/organic pollutants, radioactive Azolla and Spirodela . wastes and explosives. 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The aquatic and wetland plant species possess heavy metals and have been used in abatement exorbitant effi ciency to remove various inorganic of heavy metals. Submerged species including and organic contaminants including heavy met- Potamogeton crispus (pondweed), Potamogeton als, radionuclides, nutrients, explosives and pectinatus (American pondweed), Ceratophyllum hydrocarbons from wastewaters. The removal of demersum (coontail or hornwort), Vallisneria contaminants varies from species to species and spiralis, Mentha aquatica (water mint) and is also dependent upon concentration of the con- Myriophyllum spicatum (Eurasian watermil- taminant and duration of exposure. The present foil) also bear the potential for extraction of chapter highlights the variety of contaminants metals from water as well as sediments. removed by aquatic plants. Well studied plant Semiaquatic/emergent plant species such as species in each category are also listed (Fig . 2.1 ). Typha latifolia (cattail), Phragmites (common reed) and S cirpus spp. (bulrush) also possess metal-removing abilities (Dhir et al. 2009 ; 2.1 Contaminants Removed Dhir 2010). by Aquatic Plants 2.1.1.2 Explosives 2.1.1 Inorganic Contaminants Submerged and emergent aquatic plant species including Elodea Michx . (elodea), Phalaris sp. (canary 2.1.1.1 Heavy Metals grass), Ceratophyllum demersum , Potamogeton Heavy metals form one of the largest categories nodosus and Sagittaria latifolia (arrowhead) have of contaminants that are effi ciently removed by demonstrated the capacity to remove explosives aquatic plants. Living and nonliving biomass of such as 2,4,6-trinitrotoluene (TNT), hexahydro- aquatic plants treat heavy metals in a sustainable 1,3,5-trinitro-1,3,5-triazine (RDX) and octahydro- way. Aquatic macrophytes, irrespective of free- 1,3,5,7-tetranitro-1,3,5,7- tetrazocine (HMX) from fl oating, submerged or emergent plant species, contaminated groundwater (Dhir et al. 2009 ) sequester heavy metals (Tables 2.1 , 2.2 and 2.3 ). (Table 2.4 ). Free-fl oating aquatic plant species, namely, Eichhornia crassipes (water hyacinth), Salvinia 2.1.1.3 Radionuclides herzogii and Salvinia minima (water ferns), Removal of radionuclides such as 137 Cs, 60 Co and Pistia stratiotes (water lettuce), Nasturtium 54 Mn by submerged and emergent aquatic officinale (watercress), Spirodela intermedia plant species including Potamogeton lucens , and Lemna minor (duckweeds) and Azolla pin- Potamogeton perfoliatus , Nuphar lutea , Nitel- nata (water velvet), possess potential to scavenge lopsis obtusa, Phragmites australis, Typha

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 21 DOI 10.1007/978-81-322-1307-9_2, © Springer India 2013 Heavy metals (Cr, Co, Ni, Cu, Pb, Se, Hg, Zn, Al, Cd, Ag, As, Au)

Nutrients (nitrogen, phosphorus, sodium, potassium) Free-floating

Inorganic Radionuclides (137Cs, 60Co, 238U, 90Sr)

Aquatic species Submerged Herbicides, Pesticide, (organochlorine compounds), Organic chlorinated solvents

Explosives (TNT, RDX) Emergent

Dyes Others

Polyaromatic hydrocarbons

TDS, BOD, COD, hardness, suspended solids

Fig. 2.1 Major categories of contaminants removed by aquatic plants species

Table 2.1 Free-ﬂ oating aquatic macrophytes with heavy metal accumulation potential Plant species Heavy metals Accumulation References Azolla ﬁ liculoides Pb 228 mg kg−1 dry wt. Zayed et al. (1998 ) Cd 2,600–9,000 mg kg−1 dry wt. Benaroya et al. (2004 ) Cu 62 mg kg−1 dry wt. Arora et al. (2006 ) Zn 48–1,200 mg kg −1 dry wt. Taghi Ganji et al. (2005 ) Ni 1,000 mg kg−1 dry wt. Azolla caroliniana Hg 578 mg kg−1 dry wt. Bennicelli et al. (2004) Cr 356 mg kg −1 dry wt. Rahman and Hasegawa ( 2011 ) As 284 mg kg−1 dry wt. Pistia stratiotes Hg 156 ng kg−1 dry wt. Maine et al. (2004 ) Cr 800–1,600 mg kg−1 dry wt. Miretzky et al. (2004 ) Cu ~1,000 mg kg−1 dry wt. Molisani et al. (2006 ) Salvinia cucullata Cd 1,636.1 μg g−1 dry wt. Phetsombat et al. (2006 ) Pb 14,305.6 μg g−1 dry wt. Salvinia natans Cr 10.6 mg kg−1 dry wt. Dhir et al. (2008 ) Zn 4.8 mg kg−1 dry wt. Spirodela polyrhiza As 400–900 mg kg −1 dry wt. Zhang et al. (2011 ) Cr Eichhornia crassipes Cr 4,000–6,000 mg kg−1 dry wt. Hu et al. (2007 ) Cu 6,000–7,000 mg kg−1 dry wt. Molisani et al. (2006 ) Cd 2,200 μg kg−1 dry wt. Zhu et al. (1999 ) Arsenite 909.58 mg kg−1 dry wt. Delgado et al. (1993 ) Arsenate 805.20 mg kg−1 dry wt. Low et al. (1994 ) Ni 1,200 mg kg−1 dry wt. Zn 10,000 mg kg −1 dry wt. Hg 1,000 ng kg−1 dry wt. Lemna gibba As 1,021 mg As kg−1 dry wt. Mkandawire and Dudel (2005 ) Cd 14,000 mg Cd kg−1 dry wt. Mkandawire et al. (2004a, b) Ni 1,790 μg Ni kg−1 dry wt. 2.1 Contaminants Removed by Aquatic Plants 23

Table 2.2 Submerged aquatic macrophytes with heavy metal accumulation potential Plant species Heavy metals Accumulation References Ceratophyllum submersum Ni 489–774 mg kg−1 dry wt. Kara (2010 ) Ceratophyllum Arsenate 862 μg As g−1 dry wt. Xue et al. (2012 ) demersum L. Arsenite 963 μg As g−1 dry wt. Saygideger et al. (2004 ) Pb 1,143 μg g−1 dry wt. Osmolovskaya and Cr 149 mg kg−1 dry wt. Kurilenko (2005 ) Myriophyllum Co 1,675 mg kg−1 dry wt. Wang et al. (1996 ) spicatum Ni 1,529 mg kg−1 dry wt. Sivaci et al. (2004 ) Cu 766 mg kg−1 dry wt. Lesage et al. (2008 ) Zn 2,883 mg kg−1 dry wt. Potamogeton Cd 596 mg kg−1 dry wt. Rai et al. (2003 ) pectinatus Pb 318 mg kg−1 dry wt. Tripathi et al. (2003 ) Cu 62.4 mg kg−1 dry wt. Singh et al. (2005 ) Zn 6,590 mg kg−1 dry wt. Mn 16,000 mg kg −1 dry wt. Hydrilla Cu 770–3,0830 mg kg −1 dry wt. Srivastava et al. (2011 ) verticillata As 121–231 mg kg−1 dry wt.

Table 2.3 Emergent species with heavy metal accumulation potential Plant species Heavy metals Accumulation References Typha latifolia As 1,120 μg g −1 dry wt. Ye et al. (1997 ) Zn 1,231.7 mg kg−1 dry wt. Qian et al. (1999 ) Cu 1,156.7 mg kg −1 dry wt. Nguyen et al. (2009 ) Ni 296.7 mg kg−1 dry wt. Manios et al. (2003 ) and Afrous et al. (2011 ) Typha angustifolia Pb 7,492.6 mg Pb kg −1 dry wt. Panich-pat et al. (2005 ) Elodea densa Hg 82–177 ng Hg g−1 dry wt. Molisani et al. (2006 ) Phragmites australis As 119.55 mg kg−1 dry wt. Windham et al. (2001 , 2003 ) Hg 6.23 mg kg −1 dry wt. Afrous et al. (2011 ) Scirpus maritimus As 65.25 mg/kg Afrous et al. (2011 ) Hg 2.23 mg/kg Spartina alterniﬂ ora As, Hg, Cu, Pb Al, 0.3–7.2 mg As kg−1 dry wt. Carbonell et al. (1998 ) Fe, Zn, Cr, Se Ansede et al. (1999 ) Windham et al. (2001 , 2003 ) Spartina patens Cd, As 250 mg Cd g−1 dry wt. Zayed et al. (2000 ) Carbonell et al. (1998 )

latifolia , Elodea canadensis , Ceratophyllum phosphorus from hydroponic systems and micro- demersum and Myriophyllum spicatum have been cosm (Dhir et al. 2009 ). noted (Dhir et al. 2009 ) (Table 2.5 ).

2.1.1.4 Ions/Nutrients 2.1.2 Organic Contaminants Aquatic plant species such as Ceratophyllum demersum , Potamogeton crispus , Eichhornia Aquatic plant species possess potential to remove, cras-sipes , Elodea nuttallii and Elodea canaden- sequester and transform organic contaminants. sis showed potential for effective removal of Uptake and accumulation of organophosphorus excess of inorganic nutrients such as nitrogen and and organochlorine compounds, chlorinated 24 2 Aquatic Plant Species and Removal of Contaminants

Table 2.4 Aquatic plant species with potential for removing explosives Plant species Contaminants References Myriophyllum aquaticum TNT, RDX, HMX Best et al. (1997 , 1999a , b ) Hughes et al. (1997 ) Rivera et al. (1998 ) Pavlostathis et al. (1998 ) Bhadra et al. (1999 , 2001 ) Myriophyllum spicatum TNT Hughes et al. (1997 ) Potamogeton nodosus TNT, RDX Best et al. (1997 , 1999b ) Bhadra et al. (1999 ) Ceratophyllum demersum TNT, RDX Best et al. (1997 , 1999b ) Bhadra et al. (2001 ) Elodea canadensis RDX, HMX Rivera et al. (1998 ) Best et al. (1999a , b ) Phalaris arundinacea TNT, RDX Best et al. (1999a , b ) Typha angustifolia TNT, RDX Best et al. (1999a , b ) Sagittaria latifolia TNT, RDX Best et al. (1997 ) Bhadra et al. (2001 ) Scirpus cyperinus TNT, RDX Best et al. (1997 , 1999a , b )

Table 2.5 Aquatic plant species with the potential for accumulating radionuclides Plant species Contaminant References Lemna minor 140 La, 99 Tc, 60 Co Hattink et al. (2000 ) Hattink and Wolterbeek (2001 ) Weltje et al. (2002 ) Popa et al. (2006 ) Lemna gibba 60 Co, 32 P, 134 Cs El-Shinawy and Abdel-Malik (1980 ) Azolla caroliniana 137 Cs, 60 Co Popa et al. (2004 ) Ceratophyllum demersum 137 Cs, 60 Co, 32 P, 60 Co, 134 Cs, 89 Sr El-Shinawy and Abdel-Malik (1980 ) Abdelmalik et al. (1980 ) Shokod’Ko et al. (1992 ) Bolsunovski˘ et al. (2002 ) Potamogeton pectinatus 238 U, 137 Cs, 90 Sr Kondo et al. (2003 ) Potamogeton lucens 90 Sr Bolsunovski˘ et al. (2002 ) Elodea canadensis 137 Cs, 90 Sr, 241 Am Shokod’Ko et al. (1992 ) Bolsunovski˘ et al. (2002 ) Bolsunovsky et al. (2005 )

solvents, hydrocarbons, explosives and pharma- 2.2.1.1 Duckweeds ceuticals by aquatic plants have been reported Duckweeds are small (1–15 cm), free-fl oating (Dhir et al. 2009 ) (Table 2.6 ). aquatic angiosperms. They are monocotyledons belonging to the family Lemnaceae . They have worldwide distribution in nutrient-rich waters of 2.2 Major Plant Species temperate and tropic zones. Duckweed consists of four genera: 2.2.1 Free-Floating Species Lemna Spirodela Some of the species well studied for their phytore- Wolffi a mediation potential have been listed below (Fig. 2.2 ). Wolffi ella 2.2 Major Plant Species 25

Table 2.6 Aquatic plant species with the potential for removing/accumulating various organic contaminants Plant species Contaminant References Eichhornia Ethion, dicofol, cyhalothrin, Roy and Hanninen (1994 ) and Xia et al. (2002a , b ) crassipes pentachlorophenol Lemna gibba Phenol, 2,4,5-trichlorophenol Hafez et al. (1998 ), Ensley et al. (1994 ), Sharma (TCP) et al. (1997 ) and Tront and Saunders (2006 ) Lemna minor 2,4,5-trichlorophenol (TCP), Day and Saunders (2004 ), Tront and Saunders halogenated phenols ( 2006 ), Tront et al. (2007 ) Spirodela Organophosphorus and organochlorine Gobas et al. (1991 ), Rice et al. (1997 ) and Gao et al. oligorrhiza compounds (o,p′-DDT, p,p′-DDT), (2000a , b ) chlorobenzenes Myriophyllum Simazine, o,p-2 DDT, p,p-2 Knuteson et al. (2002 ), Nzengung et al. (1999 ) and aquaticum DDT, hexachloroethane Gao et al. (2000a ) (HCA), perchlorate Potamogeton crispus Phenol Barber et al. (1995 ) Ceratophyllum Organophosphorus and Gobas et al. (1991 ), Wolf et al. (1991 ), Rice et al. demersum organochlorine compounds, ( 1997 ) and Gao et al. (2000a , b ) chlorobenzenes Elodea canadensis Phenanthracene, organophosphorus Gobas et al. (1991 ), Wolf et al. (1991 ), Rice et al. and organochlorine compounds, ( 1997 ), Machate et al. (1997 ), Gao et al. (2000a , b ), chlorobenzenes Hexachloroethane Nzengung et al. (1999 ), Gao et al. (2000a ) and (HCA), DDT, Carbon tetrachloride Garrison et al. (2000 ) Pontederia cordata Oryzalin (herbicide) Fernandez et al. (1999 ) Scirpus lacustris Phenanthracene Machate et al. (1997 )

Fig. 2.2 Free-ﬂ oating aquatic plant species: (a ) Lemna , ( b ) Eichhornia , (c ) Azolla and ( d ) Salvinia

Lemna is the largest genera among all duck- Unique properties of the species which estab- weed species. They are small ubiquitous plants lish them as ideal phytoremediation agents and whole plant body is reduced to form a ﬂ at mainly include: small leaf-like structure called frond which • Fast growth and multiplication (doubling consists of leaﬂ ets and root-like structure. The biomass between 0.2 and 7 days) ideal growth conditions are water temperatures • High bioaccumulation potential. between 6 and 33 °C and pH ranging from 5.5 • Ability to transform or degrade contaminants. to 7.5 (Mkandawire and Dudel 2007 ). They • Regulate chemical speciation. reproduce asexually. These are easy to culture • Capacity to treat variable contaminants (both in laboratory and hence are material of choice organic and inorganic). for ecotoxicological investigations (Prasad • Some species have been commercially et al. 2001 ). exploited to recover valuable metals like Au 26 2 Aquatic Plant Species and Removal of Contaminants

and Ag from wastewater and mining wastes waters and showed tolerance upto concentrations (Obek and Sasmaz 2011 ). of 2 mg L−1 without any adverse effects on biomass Average yield of Lemna in uncontaminated production ( Del- Campo Marıń and Oron 2007 ). waters corresponds to 20–50 g m−2 d−1 dry biomass, Exposures to higher concentrations of most of these while 200 g −2 d −1 dry biomass has been reported metals (Cu, Cd, Ni, Zn) inhibited growth (around under laboratory conditions and tropical regions. 50 %) measured in terms of biomass production and In Lemna species, particularly L . minor and physiological changes such as photosynthetic and L . gibba , growth rate of 0.6 d−1 has been noted respiration rate (Khellaf and Zerdaoui 2010a , b ). under ideal media and nutrient conditions. Lemna minor has been studied extensively High biomass production rate contributes to and studies have demonstrated its potential for high bioaccumulation potential (Mkandawire treatment of wastewater from oil refi nery, sewage and Dudel 2007 ). Duckweeds possess capacity to water systems and municipal outlets (Azeez and remove wide range of inorganic and organic Sabbar 2012 ). The improvement in water quality contaminants such as heavy metals, radionuclides, has been achieved by reducing heavy metals, nutrients, pesticides and explosives from domestic, turbidity, biochemical oxygen demand (BOD), municipal and industrial wastewaters. total soluble solids (TSS), total alkalinity, total 3− suspended solids, phosphate ( PO4 -P), sulphide, Inorganic Contaminants sulphate, nitrates and phenols (El-Kheir et al. 2007 ). Lemna species, L . minor , L . gibba and L . trisulca , Lemna minor and L . gibba have also shown showed removal of heavy metals, namely, Hg, capacity to treat rare earth elements (REE) such Pb, Cr, Cu, Zn, Al, Cd, Ag, As and Au, from as lanthanum and radioactive elements such as wastewaters (Kara and Kara 2005 ; El-Kheir et al. uranium (U) (Cheng et al. 2002 ). 2007; Kara 2010 ; Rahman and Hasegawa 2011 ; Lemna sp. also showed an effi cient antioxi- Arenas et al. 2011 ; Obek and Sasmaz 2011 ; dant machinery to curtail oxidative stress caused Uysal and Taner 2011 ; Parra et al. 2012 ; Sasmaza by abiotic stresses including heavy metal expo- and Obek 2012 ; Singh et al. 2012a , b ). The sure. This includes increased level of antioxi- removal effi ciency varies from 3 to 30 % dant molecules—ascorbate and glutathione—as depending on the element. Nutrient enrichment well as activities of antioxidant enzymes, − 2− (P, NO 3 –N and SO 4 ) of the medium negatively namely, ascorbate peroxidase, dehydroascor- affects the metal accumulation potential, but bate reductase and ascorbate free radical (AFR) enhances the metal tolerance capacity of duck- reductase (Paola et al. 2007 ). Some studies in weeds and hence growth (Leblebici and Aksoy L. minor suggested that callose acts as a barrier 2011 ). Studies with Lemna gibba indicated to prevent metal penetration and hence stress, reduction in metal accumulation after addition of though it is not well accepted. Lead-induced 3− PO4 . This can be attributed to strong interaction synthesis and deposition of callose was noted among chemical components and competition among in roots of L . minor. Though continuous callose ions in natural aquatic environment. Arsenic bands, small clusters or incomplete bands in the (As(V)) is an analog of phosphate and competes newly formed and anticlinal cell walls (CWs) for the same uptake carriers in the plasmalemma. could form an effi cient barrier for Pb penetra- Studies indicate competitive inhibition of As(V) tion, it is noted that such callose arrangement by phosphate (Mkandawire et al. 2004a, b; within root CWs ineffi ciently protect the proto- Mkandawire and Dudel 2005 ). plast from Pb penetration and might not be The tolerance capacity of the plant varied for enough for a successful blockade of the stress each metal. Lemna gibba tolerated Cu and Ni at con- factor penetration (Samardakiewicz et al. 2012 ). centrations 0.3 and ≤0.5 mg L−1 , while L . minor toler- Biosynthesis of the cytoplasmic Hsp70 protein, ated Cd, Cu, Ni and Zn at concentrations of 0.4, 0.4, a nonspecifi c and sensitive detector of stress in 3 and 15 mg L −1, respectively (Khellaf and Zerdaoui fronds exposed to lower doses of stressors 2010a , b ). Lemna gibba showed effi ciency for including Cd have been detected in L . minor removing boron (B) from polluted and desalinated (Tukaj et al. 2011 ). 2.2 Major Plant Species 27

Organic Contaminants macrophyte biomass and heavy metal ions and L . minor accumulates trace-organic contaminants protons present in water. S . polyrhiza showed and ultimately served as a sink for these materials potential for degrading nitrophenols. The bacte- in the natural environment. Uptake rate (pH ria isolated from the roots or rhizosphere region values 6–9) and plant activity showed a positive of S . polyrhiza contributed to the accelerated degra- correlation. Plant showed capacity for removing dation of the three NPs, namely, 2-nitrophenol and tolerating herbicides, namely, isoproturon (2-NP), 4-nitrophenol (4-NP) and 2,4-dinitrophenol and glyphosate, 2,4,5-trichlorophenol (TCP) and (2,4-DNP) (Kristanti et al. 2012 ). organic residues including commercial solvent and resin such as phenol, pyridine and formalde- 2.2.1.2 Eichhornia crassipes hyde present in industrial wastewaters (Tront (Water Hyacinth) et al. 2001 ; Tilaki 2010 ; Dosnon-Olette et al. Commonly referred as the ‘world’s most noxious/ 2011 ). Uptake rates were linearly correlated to troublesome aquatic weed’. It is a native to tropical fraction of contaminant in protonated form. and subtropical South America and is now wide- Lemna minor showed effi cient uptake capacity spread in all tropic climates. It is a free- fl oating, for pesticides—copper sulphate (fungicide), perennial aquatic fern belonging to family fl azasulfuron (herbicide) and dimethomorph Pontederiaceae. It forms dense mats in the water (fungicide). Duckweed demonstrated the greatest and mud. It is also referred as ‘bull hyacinths’. potential to transform and hence degrade (50– It fl ourishes and reproduces fl oating freely on 66 %) DDT isomers o,p′-DDT and p,p′-DDT. the surface of water or it can also be anchored in The decay profi le of DDT followed fi rst-order mud. It grows in ponds, canals, freshwater and kinetics. Reduction of the aliphatic chlorine coastal marshes and lakes. It multiplies by veg- atoms of DDT was noted as the major pathway etative reproduction, which allows the plant to for transformation. In contrast, L . minor showed quickly colonize large areas in relatively short susceptibility to hydrophobic organic compounds periods of time (Wolverton and McDonald such as synthetic antifungal drug ketoconazole. 1979 ). The plant can double its population in Exposure to ketoconazole (0.3–0.6 mg L−1 ) 6 days. The genus Eichhornia comprises seven for 168 h affected growth rate, dry weight and species, among which E . crassipes is the most root length (Haeba and Bláha 2011 ). Lemna common. minor showed capacity to remediate explosives, Management of this weed is an issue of serious mainly TNT (Feuillebois et al. 2006 ; Tront and concern all over the world plant because of its Saunders 2006 ). huge vegetative reproduction and high growth rate (Jafari 2010). Therefore, studies suggested Other Duckweeds some potential uses of the plant. These mainly Spirodela (greater duckweed) and Wolffi a species include its utilization as follows: have been reported to accumulate and hence (a) Phytoremediation agent treat metal-contaminated waters (Mkandawire (b) Biosorbent for toxic metals et al. 2004a , b ; Mkandawire and Dudel 2005 ; (c) Resource for power generation and biogas Rahman et al. 2007 , 2008 ; Alvarado et al. 2008 ; production Leblebici and Aksoy 2011 ; Zhang et al. 2011 ). (d) Compost S . polyrhiza , S . intermedia and Wolffi a showed (e) Animal fodder/fi sh feed As, Pb and Cd accumulation and tolerance effi - (f) Pulp material for paper production ciency (Mkandawire et al. 2004a , b ; Mkandawire (g) Production of fi breboards, low cost roofi ng and Dudel 2005 ; Rahman et al. 2007 , 2008 ; material, indoor partitioning, etc. Alvarado et al. 2008 ; Zhang et al. 2011 ). The (h) Formulations of medicines adsorption process followed fi rst-order kinetics. (i) Biomass can be used for metal recovery Biosorption mechanism causes ion exchange Use of water hyacinth in wastewater treatment between monovalent metal ions present in is recommended because of its 28 2 Aquatic Plant Species and Removal of Contaminants

1. Enormous biomass production rate several advantages including cost-effectiveness, 2. High tolerance to pollution high effi ciency, minimization of chemical/bio- 3. Absorption capacity for variable contaminants logical sludge and regeneration of biosorbent like heavy metal and nutrients with possibility of metal recovery. Exposure to high concentrations of heavy Inorganic Contaminants metals such as Cu (1 mg L−1 ) and Se (5 and 10 mg E . crassipes attracted considerable attention L−1 ) caused marked changes in physiology of the because of its ability to grow well in polluted water plant (Hu et al. 2007; Buta et al. 2011 ). Higher together with its capacity of accumulating heavy concentrations of heavy metals adversely affected metal ions (Maine et al. 2001 ; So et al. 2003 ; Lu pigment production (chlorophyll a, chlorophyll et al. 2004 ; Ghabbour et al. 2004 ; Odjegba and b, total chlorophyll), protein, starch, soluble pro- Fasidi 2006 ). Plants absorb depending upon their tein and free amino acids. Oxidative stress in affi nity towards the particular metal. Based on chloroplasts brings damage to membranes by absorption and accumulation mechanisms, E . impacting the normal physiological function of crassipes render services of cleaning of water proteins and lipids. The loss in pigment concen- body, sewage and sludge ponds from heavy metal trations results from heavy-metal-mediated per- and nutrient contamination. E . crassipes possess oxidation of chloroplast membranes. The capacity to treat industrial and municipal waters decrease in the total starch contents could result contaminated with Pb, As, Hg, Zn, Se, Cr, Cd, Ni from poor performance of photosystems and and Cu (Win et al. 2002 , 2003 ; Dixit and Tiwari inhibition of the Calvin cycle enzymes (Clijsters 2007 ; Hussain et al. 2010 ; Mahamadi 2011 ; Mane et al. 1999). The poor protein formation could be et al. 2011 ; Mokhtar et al. 2011 ; Rahman and related to disruption of nitrogen metabolism from Hasegawa 2011 ; Murithi et al. 2012 ). High rate of high doses of metals. Since nitrogen is one of the metal accumulation safely places it in the category primary essential nutrients involved as a constitu- of metal hyperaccumulator. Roots tend to accumu- ent of biomolecules such as nucleic acids, nitro- late a higher amount of metal than shoots due to gen bases, coenzymes and proteins, any deviation translocation process. At lower concentrations, in these constituents would inhibit the growth metal accumulation was observed in the roots and and yield of plants (Vitória et al. 2011 ). leaves, while at higher concentrations, metal trans- It is considered as the most effi cient aquatic location from roots and leaves drained into the plant for wastewater purifi cation since it bears metallic ions and deposits them in different parts potential for removing vast range of pollutants of the plant body petiole. It was deduced that the such as heavy metals, organic substances, nutrients carboxylate group on the surface of the biomass (nitrate, ammonium, phosphorus), total suspended facilitate metal adsorption (Dixit et al. 2010 ). solids (TSS), total dissolved solids (TDS), turbidity Sorption of metal ions depends on contact time, from municipal and industrial (textile, metallur- pH and concentration. The sorption data fi tted gical, pharmaceutical, paper) wastewater, sewage well with the Langmuir and Freundlich models. effl uents and domestic wastewater (Kutty et al. Acid and base treatment affected metal uptake. 2009 ; Muthunarayanan et al. 2011 ; Yadav et al. 2011 ; Acidic treatment increased the uptake capacity of Ajayi and Ogunbayo 2012 ; Kumar et al. 2012 ). water hyacinth roots for Cr6+ , whereas the removal Water hyacinth remediates aquatic environ- of Cr3+ was lower (Narain et al. 2011 ). ments contaminated with the lanthanide metal, Activated carbon and ash derived from water europium (Eu(III)). Highest concentration of Eu(III) hyacinth possess potential for removing metal is adsorbed onto the surface of the roots. NMR ions (Kadirvelu et al. 2005). Mahmood et al. and IR spectroscopy established that carboxylate (2010 ) reported that ash of water hyacinth also groups are the dominant functional groups respon- showed capacity for hyperaccumulation of Pb, sible for binding Eu(III) to the roots of water Zn, Cr, Zn, Cu and Ni. Plant-derived ash offers hyacinth. 2.2 Major Plant Species 29

Organic Contaminants dorsal lobe cavity of its leaf helps in nitrogen Dyes are major pollutants present in the effl uents fi xation. The biomass is also used as a biofertilizer of the textile, leather, food processing, dyeing, or as a feed supplement for aquatic and terrestrial cosmetics, paper and dye-manufacturing indus- animals (Costa et al. 1999 ). tries. They are synthetic aromatic compounds which are embodied with various functional Inorganic Contaminants groups. Dye-containing wastewater causes serious Azolla species, namely, A . caroliniana , A . fi liculoi- water pollution problems by hindering light pen- des and A . pinnata , possess high capacity to accu- etration. Most of the dyes resist biological oxida- mulate toxic elements such as Hg, Cd, Cr, Cu, Ni, tion, are stable against light and oxidizing agents, Zn, Pb and As (Bennicelli et al. 2004 ; Zhang et al. and require tertiary treatment; hence, their removal 2008a , b ; Rai and Tripathi 2009 ; Rahman and by conventional treatment procedures is not easy. Hasegawa 2011; Taghi ganji et al. 2012 ) and can be Eichhornia crassipes showed effi ciency for remov- used to remove contaminants from wastewater/ ing dyes and degrading ~90 % of red RB, black B industrial effl uents, domestic wastewater and pre- and malachite green. The roots of water hyacinth cious metals such as gold (Au) from aqueous solu- have shown biosorption/accumulation of ethion tion (Bennicelli et al. 2004 ; Rakhshaee et al. 2006 ; and reactive dyes (Xia and Ma 2006 ; Gopinath Smadar et al. 2011 ). The initial binding and et al. 2012 ; Shah et al. 2010 ). Promising attributes exchange of heavy metal ions to insoluble constitu- of water hyacinth include its tolerance to dye and ents in the Azolla matrix most probably involves dye absorption along with good root development, cell wall charged groups (such as carboxyl and low maintenance and ready availability in contam- phosphate). Pectin and cellulose are important inated regions. The sorption process followed polysaccharides constituent of plant cell walls, fi rst-order kinetics. The negative value of the free made of fragments of polygalacturonic acid chains, energy change indicated the spontaneous nature of which interact with Ca2+ and Mg2+ (exchange ions the sorption and confi rms the affi nity between the with heavy metals) to form a three-dimensional sorbent and the dye cations. polymer by (−COO)2 Ca and or (−COO)2 Mg bind- Water hyacinth signifi cantly reduced naphtha- ing as the ion exchanging bases (Sood et al. 2004 ; lene (a polyaromatic hydrocarbon) (~45 %) present Taghi ganji et al. 2005 ). A correlation between in wastewater and wetlands. Microbial activity metal adsorption and the availability of carboxyl of rhizospheric bacteria enhanced removal of groups of galacturonic acid, the principal constitu- naphthalene. Uptake by water hyacinth revealed ent of pectin, have been reported. Methylation, a biphasic behaviour: a rapid fi rst phase completed demethylation of carboxyl groups and pectinase after 2.5 h and a second, considerably slower treatment demonstrated that pectin of the Azolla rate, phase (2.5–225 h) (Nesterenko- Malkovskaya cell wall is the major metal binding site. et al. 2012 ). Azolla caroliniana and Azolla pinnata showed capacity to purify polluted waters and ameliorate 2.2.1.3 Azolla (Water Fern) industrial effl uents (thermal power, chlor-alkali Azolla (Azollaceae) is a small, free-fl oating water and coal mine effl uent). This is achieved by fern commonly found in tropical and temperate reducing signifi cant levels of electrical conduc- freshwater ecosystems. It is widely distributed in tivity (EC), TDS, BOD, chemical oxygen demand paddy fi elds, rivers, ponds and lakes. Plant body (COD), hardness, acidity and sodium and potas- is composed of fronds which are triangular or sium content. Native biomass and chemically polygonal and fl oat on the water surface individ- modifi ed biosorbent, i.e. hydrogen peroxide Azolla ually or in mats. Frond consists of a main stem sorbent (HAS), showed good sorption capacities growing at the surface of the water, with alternate for Cs and Sr (pH 8 and 9). Microwave reaction leaves and adventitious roots at regular intervals showed complete removal of metallic Ag and along the stem. Anabaena azollae that lives in the Pb nanoparticles from the polluted solution using 30 2 Aquatic Plant Species and Removal of Contaminants

A . ﬁ liculoides. Adsorption and reduction combined BTEX. Aquatic plants increase the surface area of using microwave radiation can be applied for the water/nonaqueous phase interface, making removing and recycling metallic ions from contam- more of the petroleum hydrocarbons susceptible inated water and industrial wastewater. Reduction to attack by microbes. Photolysis by plant gener- of the metallic ions was accomplished by the ates free radicals, such as the alkylperoxyl radical, plant matrix without the need of an external that can oxidize aromatic rings and side chain reducing agent. The proteins or sugar alcohols in structures of petroleum hydrocarbons. The solu- the plant matrix serve as the reducing agents. bility of non-volatile hydrocarbons increases at Exposure to high metal concentrations present higher temperatures making them more available in the wastewaters particularly Zn plating to microbes. Supplementation with inorganic industrial efﬂ uent affected root growth and other nutrients can greatly increase the rate of diesel biochemical parameters such as chlorophyll, degradation in soil. carotenoid, polyphenol, protein, RNA, DNA and Pesticides such as monocrotophos accelerate − 3− − nutrient (NO3 and PO 4 ) content in the fronds of the formation of reactive oxygen species, i.e. O2

Azolla caroliniana (Deval et al. 2012 ). Exposure and H2 O2 in cells, via lipid peroxidation in to high Cd and Cu (0.2, 1 and 2 mM) concentra- A . fi liculoides. This results in physiological and tions affected photosystem II activity and altered biochemical alterations in growth and defence photochemical yields (Fv/Fm) in A . fi liculoides system such as chlorophyll and carotenoid content. and A . caroliniana (Sánchez-viveros et al. 2010 ; Oxidative stress induced proline accumulation Gonzalez-Mendoza et al. 2011 ). and activity of superoxide dismutase (SOD) and peroxidase (POD) (Chris et al. 2011 ). Organic Contaminants Olive mill wastewater (OMWW) contains high Azolla fi liculoides showed capacity for removal of amounts of organic compounds (sugars, polyphenols, hydrocarbons from aquatic environment (Cohen tannins, polyalcohols, pectins and lipids). The et al. 2002 ). The presence of aromatic hydrocar- toxicity of OMWW is also due to its high phenolic bons such as benzene, toluene, ethylbenzene and content. Azolla showed capacity to remove poly- xylene, which are together termed as BTEX, con- phenols and chemical oxygen demand (COD) from tribute to toxicity of diesel (Lohi et al. 2008). olive mill wastewater (OMWW) collected from the Biodegradation of diesel compounds depends on traditional (TS) and continuous (CS) extraction factors such as the accessibility to microbes, the systems (Ena et al. 2007 ). capacity of the microbial community for hydro- Azolla fi liculoides Lam. was able to survive in carbon utilization and the inorganic nutrient com- drug-contaminated waters. Plants showed active position of the environment. Azolla pinnata removal of drug sulphadimethoxine (S), a persistent showed ability to degrade hydrocarbon from die- antibiotic from the medium (Fornia et al. 2002 ). sel. Concentrations of xylenes and ethylbenzene This caused alteration in growth (biomass yield) were 50–100 times lower. Azolla plants release a and N2 -fi xation in N-free mineral medium. Drug consortium of bacteria capable of signifi cantly uptake and degradation rates increase with S lowering levels of diesel fuel pollution. Enhan- concentrations in the culture medium. Azolla cement of diesel degradation in the plant-added caroliniana showed ability to grow and dissipate plots was due to the release of bacteria (bioaug- phenanthrene (PHE) by using bioaugmentation with mentation) and physiochemical improvement of hydrocarbonoclastic microorganisms (Bacillus the plot conditions (biostimulation) (Al-Baldawi stearothermophilus and Oscillatoria sp.) (Castro- et al. 2012 ). Plants synthesize a variety of enzymes Carrillo et al. 2008 ). that help in degradation of petroleum aliphatic and aromatic hydrocarbons. Some microbial deg- 2.2.1.4 Pistia stratiotes (Water radative enzymes induced by plant compounds Lettuce) can co-oxidize compounds. Phosphate supple- Pistia is a genus belonging to family Araceae mentation appeared to stimulate degradation of and comprises of a single species, P . stratiotes . 2.2 Major Plant Species 31

It fl oats on the surface of the water with its Organic Contaminants roots hanging beneath floating leaves. It is a Pistia stratiotes L. showed ability to accelerate common aquatic weed in the United States. degradation of aromatic compounds in the rhi- Dense mats degrade water quality by blocking zosphere. It could promote growth of microbe, the air–water interface, reducing oxygen lev- retain a large microbial population in the rhizo- els in the water and thus threatening aquatic sphere and efficiently transport oxygen to life. stimulate the rhizospheric microbial activity, leading to phenol, aniline and 2,4-dichlorophe- Inorganic Contaminants nol degradation. It could accelerate removal of Pistia stratoites showed capacity for phytofi ltra- compounds through mechanisms such as (1) tion of toxic heavy metals such as As, Cd, Cu, Ni, retaining a large population of the aromatic Zn, Pb, Cr, Mn and Co from contaminated waters compound degraders, (2) stimulating bacterial and urban sewage (Maine et al. 2001 ; Miretzky growth and degradation activity and (3) remov- et al. 2006; Espinoza-Quiñones et al. 2009 ; ing aromatic compounds directly. Plant also Venkatrayulu et al. 2009 ; Hua et al. 2011 ; Lu showed potential to remove chlorpyrifos from et al. 2011 ; Rawat et al. 2012 ; Prajapati et al. water, though higher chlorpyrifos concentra- 2012). The rate of metal translocation is slow and tions (0.5 and 1 mg L −1 ) inhibited relative most of the metal is strongly adsorbed onto root growth rates (RGR) (Prasertsup and surfaces. Exposure to higher metal concentra- Ariyakanon 2011 ). Plant showed capability to tions (Mn) (50, 200, 400 mg L−1 ), Cr (1 and lower antimicrobial drug concentration, such 10 mM) showed a decrease in relative growth as sulphonamide (sulphadimethoxine) and a rate and reduction in plant biomass (Upadhyay quinolone (fl umequine), though plant growth and Panda 2010). The metal sorption data fol- was adversely affected (Forni et al. 2006 ). lowed Langmuir and Freundlich isotherms. The adsorption process followed fi rst-order kinetics 2.2.1.5 Salvinia (Water Fern) and the mechanism involved in biosorption Salvinia is a small free-fl oating aquatic fern resulted in ion exchange between monovalent belonging to family Salviniaceae. It possesses metals as counter ions present in the macrophyte branched creeping stems bearing two types of biomass. High metal treatments also affected bio- leaves—upper green (photosynthetic) and lower chemical parameters such as chlorophylls pro- submerged (hairy) bearing sori that are surrounded tein, free amino acid and RNA, DNA content by basifi xed membranous indusia (sporocarps). along with enzymic and non-enzymic antioxi- Leaves are present in whorls at each node. The dants, thus regulating oxidative stress. genus Salvinia is comprised of 1 genus and 12 Plant species possess capacity for improving species. Salvinia minima is the smallest free-fl oat- water quality of dairy, aquaculture, sewage, indus- ing freshwater fern found in tropical and temper- trial wastewater, storm water, drinking and surface ate regions (DeBusk and Reddy 1987 ). Its wide water samples by reducing nutrients, COD, pH, distribution, faster growth rate and easy handling turbidity, dissolved oxygen (DO), BOD, phosphate make it a potential candidate for phytoremediation. 3− − − (PO4 ), nitrate (NO3 ), nitrite (NO2 ), ammonia Under optimal conditions, populations of Salvinia

(NH3 ) and total Kjeldahl nitrogen (TKN). Hence, can double in size in approximately 3.5 days. its role in removal of aquatic macrophytes from Heavy metal removal potential of Salvinia sp. water bodies is recommended for effi cient water particularly S . natans is well studied (Dhir et al. purifi cation (Polomski et al. 2009; Lu et al. 2010 ; 2009 ; Dhir 2010 ; Dhir and Srivastava 2011 ). Akinbile and Yusoff 2012 ). Small-scale surface Salvinia natans is an established bioaccumulator fl ow constructed wetlands with Pistia stratoites , of metals and has the potential to be used in Phragmites australis, Typha orientalis and Ipomoea constructed wetland systems for wastewater aquatica exhibited higher nitrate removal effi cien- treatment as it has a very high growth rate in cies from groundwater (70–99 %). nutrient-rich and stagnant waters (AbdElnaby 32 2 Aquatic Plant Species and Removal of Contaminants and Egorov 2012 ). Metal accumulation in Salvinia ment also resulted in the highest photosynthetic was higher in the roots. Salvinia demonstrated rate, chlorophyll content and anthocyanins con- the ability to withstand Al (concentrations 20 mg centrations. Nitrogen and phosphorus concentra- L−1 ), Cr (2.0 mg L−1 ), As (200 μM) and Pb tion did not infl uence carbohydrate and sugar (20–40 μM) (Gardner and Al-Hamdani 1997 ; accumulation (Al-Hamdani and Sirna 2008 ). Nichols et al. 2000; Hoffman et al. 2004 ). Metal Salvinia shows good potential for use as a bioin- accumulation increased with the addition of dicator and it can be used in the biomonitoring sulphur to the nutrient solution (Hoffman et al. of aquatic ecosystems contaminated by metals 2004 ), while increasing phosphate concentration and could be a good plant for remediation of decreased metal uptake (As) as reported in S . natans eutrophic water. and S . minima (Hoffman et al. 2004 ). Higher boron (B) accumulation in S . natans Organic Contaminants induced changes in physiological condition and Salvinia molesta showed the ability to resist diesel biomass production. Boron concentration of contaminant (8,700, 17,400, 26,000, 34,800 and 1 mg B dm−3 had no effect on the tested species, 43,500 mg L −1 ) in synthetic wastewater. 33 % of while higher concentrations of 6 and 8 mg B dm−3 the aquatic plants withered at the concentration had negative effects (Holtra et al. 2010 ). Exposure of 8,700 mg L −1 , and 100 % withered at higher to higher Cd concentrations proved toxic and showed concentration of 43,500 mg L−1 . The withering of damage in the leaves of S . auriculata (Vestena et al. plant increased with increase in concentration 2007; Wolff et al. 2012 ). Necrosis, chlorosis and (Albaldawi et al. 2011 ). ultrastructural deformities (chloroplast) such as damage to stomata, trichomes, biomass reduction and deterioration in the cell wall was noted. Lead 2.2.2 Submerged Species accumulation caused damage in roots than in leaves as indicated by the decrease in their carotenoid Submerged plants such as Potamogeton crispus content. Salvinia minima , Pb-hyperaccumulator (pondweed), Potamogeton pectinatus (American aquatic fern, showed increased accumulation of pondweed), Ceratophyllum demersum , GSH in both leaves and roots and increased the Vallisneria spiralis , Mentha aquatica (water mint) enzymatic activity of glutathione synthase (GS). and Myriophyllum spicatum (parrot feather) have Phytochelatins play an important role in protecting shown potential for accumulating metals from leaves from the detrimental effects of Pb perhaps water as well as sediments (Fig. 2.3 ). by counteracting the effect of free radicals (Estrella- Gómeza et al. 2012 ). 2.2.2.1 Ceratophyllum (Coontail Effectiveness of S . minima and S . natans in or Hornwort) + accumulating nitrogen (NH4 –N, NO3 –N), and It is a submerged, rootless, perennial plant and is phosphorus under different eutrophic environ- a cosmopolitan in distribution. It is commonly ments is reported. Salvinia growth (fresh and dry found in ponds and slow-fl owing streams. It has a weight) signifi cantly declined at NaCl concentra- high capacity for vegetative propagation and tions (3.0, 3.5 and 4.0 g L−1 ). The reduction in biomass production even under low nutritional growth coincided with a decline in CO2 assimila- conditions (Arvind and Prasad 2005 ). tion, while decrease in water potential followed increase in Na accumulation (Al-Hamdani 2008 ). Inorganic Contaminants Salvinia’s growth, expressed as frond production Ceratophyllum demersum and C . submersum and plant biomass (fresh weight), was signifi cantly showed accumulation of Cd, As mainly arsenate increased with increasing nitrogen (concentration and arsenite and Ni from hydroponic cultures from 1.0 mg L −1 to 100.0 mg L −1 ) and increasing (Kumar and Prasad 2004 ; Kara 2010 ; Matamoros of P concentration (concentration from 1.0 mg L−1 et al. 2012 ; Xue et al. 2012 ). Higher infl ux of arse- to 100.0 mg L −1) in the growth media. This treat- nate was noted in plants exposed to As solutions 2.2 Major Plant Species 33

Fig. 2.3 Submerged aquatic plant species: (a ) Ceratophyllum , (b ) Potamogeton , ( c ) Myriophyllum and ( d ) Hydrilla without the addition of phosphate (P). Metal showed potential for removal of diclofenac, accumulation by plant increased with increasing triclosan, naproxen, ibuprofen, caffeine and MCPA. treatment concentration and duration. Exposure Plants contribute to the elimination capacity of to high Pb concentrations (20, 50, 100 μg mL−1 ) microcontaminants in wetland systems through adversely affected total chlorophyll and nitrogen biodegradation and uptake processes (Matamoros contents (Larson et al. 2002 ; Saygideger et al. et al. 2012). Triclosan, diclofenac and naproxen 2004 ). Ceratophyllum demersum could recycle were removed predominantly by photodegradation, the wastewater mainly raw municipal wastewater whereas caffeine and naproxen were removed (RMW) and treated municipal wastewater (TMW) by biodegradation and/or plant uptake. The for- to be reused for irrigation purpose in agriculture mation of two major degradation products from fi elds. Plant showed good removal effi ciency ibuprofen, carboxy- ibuprofen and hydroxy- (60–90 %) for Fe, Zn, Mn, Ni, Pb and Cd from ibuprofen, is reported. TMW and RMW. C . demersum showed capabilities to remove trace elements and minerals 2.2.2.2 Potamogeton (Pondweed) (Ca, N, P, Na, K) directly from the contaminated Potamogeton sp. is an aquatic, lightly rooted and water and compost latex (diluted 200 times with partly submerged plant. It is commonly found in distilled water). C . demersum showed potential slow-moving streams, ponds and lakes. It bears for removing electrical conductivity (EC), COD, narrow, acute, fl at-margined or curly leaves. The ammonium, nitrate and phosphorous (Wang et al. biomass production rate can be as high as 100 kg 2005 ; Foroughi 2011a , b ; Foroughi et al. 2010 ). ha−1 day −1 (Schneider et al. 1999 ). The species C . demersum take up nitrate effectively from include P . cripsus and P . natans . hydroponic systems (Toetz 1971 ). C . demersum cultured in mesotrophic, eutrophic and hypertro- Inorganic Contaminants phic and Hoagland’s solutions showed changes Potamogeton pectinatus L. and Potamogeton of total N (TN) and total P (TP) concentrations malaianus Miq showed capacity for accumulating in nutrient solutions. The plant from eutrophic Cd, Pb, As, Cu, Zn and Mn (King et al. 2002 ; solution showed higher SOD and POD activities, Demirezen and Aksoy 2006 ; Fritioff and Greger showing good survival preferably under eutro- 2006 ; Anawar et al. 2008 ; Sivaci et al. 2008b ; Rahman phic condition. and Hasegawa 2011 ). Higher concentrations of metal were found in the leaves of P . pectinatus . Organic Contaminants Dead biomass of the Potamogeton sp., particu- Microcosm wetland systems (5-L containers) planted larly P . natans, possesses good sorption capacity with C . demersum along with different aquatic for Hg and hence removal from aqueous solution. species S . molesta , L . minor and E . canadensis Atomic absorption, electron microscopy and X-ray 34 2 Aquatic Plant Species and Removal of Contaminants energy dispersion analyses showed that sorption effectively reduced 2,4,6- trinitrotoluene (TNT), of Hg(II) took place over the entire biomass hexahydro-1,3,5-trinitro- 1,3,5-triazine (HMX), surface; bright spots showed high concentrations 2,4,6- trinitrobenzene (TNB) and octahydro- of Hg which may be due to surface HgO precipi- 1,3,5,7-tetranitro-1,3,5,7-tetrazocine (RDX) in tation particularly on active sites. Multilayer sorp- the groundwater. The rate of explosives removal tion of Hg(II) was noted. Sorption process occurs in the wetlands followed fi rst-order kinetics. The by two different mechanisms. A rapid uptake lagoon was very ineffective at removing RDX removing ~ 90 % of metal is followed by a slower and HMX in the contaminated groundwater. TNT passive uptake that involves diffusion into pores is believed to be degraded by submergent plant on the biomass surface. pH value affects metal species via production of nitroreductase enzymes uptake capacity and pH value of 9–10 was found which should have yielded amino derivatives to be optimum (Lacher and Smith 2002 ). It is also in the aqueous phase with a decrease in TNT suggested that dead biomass might be reducing concentrations (Best et al. 1998 ). In a similar Hg(II) to Hg(I) and/or HgO. study, plant could treat explosives-contaminated Submersed plants can be useful in reducing groundwater from the Iowa Army Ammunition heavy metal concentrations in storm water, since Plant (IAAP), Middletown. Species evaluated they can accumulate large amounts of heavy were C . demersum L. and P . nodosus Poir. Plants metals in their shoots (Fritioff et al. 2005 ). Storm were rooted in local, IAAP, sediment under water comprises rainwater and water draining continuous- fl ow conditions. Unplanted sediment from hard surfaces such as roads and roofs in served as control. Aqueous TNT and RDX con- urban areas and often contains heavy metals, in centrations decreased exponentially (fi rst-order particular Cu, Zn, Cd and Pb (Peng et al. 2008 ). kinetics). Zn, Cu, Cd and Pb present in storm water were Wetland mesocosms planted with Potamogeton taken up by P . natans . Highest accumulation is spp. and Typha sp. (Typha latifolia and T . augus- found in the roots. Cell wall-bound fraction was tifolia) showed degradation of two commonly generally smaller in stems than in leaves. The used herbicides, atrazine and alachlor. Atrazine metal concentrations in the plant tissue increased mass loss was more rapid in the emergent meso- with increasing temperature and low salinity. cosms than in the open or submergent mesocosms. Higher level of metal accumulation results in Alachlor dissipated more rapidly than atrazine toxicity. Chlorophyll levels decreased, while under all treatments. More than 50 % of the ala- anthocyanin and total phenolic concentrations chlor concentration and mass were lost within increased with exposure to high Cd concentrations 21 days under all treatments (dissipation half-life (8, 16, 32 and 64 mg L−1 ). Abscisic acid content of alachlor mass ~10–20 days). Deethylatrazine was found to increase with increased in Cd concen- (DEA), a metabolite of atrazine, was detected tration and exposure time (Sivaci et al. 2008a ). in all mesocosms (Lee et al. 1995 ; Lovett-Doust et al. 1997 ). Organic Contaminants Potamogeton spp. showed capacity for removing 2.2.2.3 Myriophyllum (Water Milfoil) organochlorine compounds including PCBs. It is a submerged plant commonly found in fresh- It also showed capacity of treating groundwater water lakes, ponds, streams and canals and appears contaminated with explosives at army ammuni- to be adapted to high nutrient environments. tion plants located at Milan. Both lagoon system It belongs to family Holoragaceae. Myriophyllum and gravel-bed system were designed. The lagoons aquaticum (parrot feather) has both submersed were planted with sago pondweed, water stargrass, and emergent leaves, with the submersed form elodea and parrot feather. The gravel- bed wetlands being easily mistaken for Myriophyllum spicatum were planted with canary grass, wool grass, sweet ( Eurasian watermilfoil ), a close relative. Leaves fl ag and parrot feather. The gravel-bed wetland are arranged around the stem in whorls of four 2.2 Major Plant Species 35 to six. The submersed leaves are 1.5–3.5-cm when they reach the water surface. The leaves are long and emergent leaves are 2–5-cm long. The 5/8-in. long, strap shaped with pointed tips and a bright-green emergent leaves are stiffer and darker distinct midrib. The green leaves are arranged in green than the submersed leaves. whorls of 4–8 and are attached directly to the stem. The leaf margins have distinct saw-toothed Inorganic Contaminants edges that are visible to the naked eye and rough Myriophyllum spicatum (parrot feather) is an to the touch. The female fl owers are single, white, effi cient plant species for the treatment of metal- with six petals, and fl oat on the surface. The male contaminated industrial wastewater as it showed fl owers are greenish and develop close to the leaf capacity to remove Co, Ni, Cu and Zn from axils near the tip of the stem. industrial effl uents (Wang et al. 1996 ; Sánchez et al. 2007 ; Lesage et al. 2008 ). Myriophyllum Inorganic Contaminants heterophyllum showed high Cd biosorption and H . verticillata has been tested for the uptake and high metal exposures resulted in loss in production remediation of As, Cu, Pb, Zn, Se and Cr from of photosynthetic pigments and total phenolic water (Carvalho and Martin 2001 ; Srivastava et al. compounds. Abscisic acid content increased with 2006 ; Bunluesin et al. 2007 ; Begum and increase in Cd concentration in Myriophyllum HariKrishna 2010 ; Dixit and Dhote 2010 ; Xue heterophyllum Michx. and exposure time (Sivaci et al. 2010 ; Rahman and Hasegawa 2011 ). Metal et al. 2008b ). uptake and accumulation in H . verticillata is dependant on both concentration of the metalloid Organic Contaminants in water and duration of exposure (Srivastava et al. Myriophyllum spicatum and Myriophyllum aquati- 2010 ), as uptake is inhibited at high phosphate con- cum showed ability to take up and transform centration. This might be due to the competitive 2,4,6-trinitrotoluene (TNT). Low concentrations of uptake of phosphate and its chemical analog As(V). aminated nitrotoluenes (2-amino-4,6-dinitrotolu- Results showed that As accumulation was about ene and 4-amino-2,6-dinitrotoluene) were observed twofold higher upon exposure to either As(V) or in the extracellular medium and tissue extracts As(III) in S-excess plants compared to that in (Hughes et al. 1997 ). Alkylphenols (APs), such as S-suffi cient and S-defi cient plants (Srivastava et al. nonylphenol (NP) and octylphenol (OP), are the 2007). As accumulation did not induce any toxic biodegradation products of ethoxylates, nonionic effects in terms of lipid peroxidation which could surfactants which have been widely used as deter- be attributed to the enhanced level of thiol metabo- gents, emulsifi ers, wetting agents, plasticizers and lites (cysteine, glutathione) and enzymatic antioxi- UV stabilizers as well as in other agricultural and dants (guaiacol peroxidase, catalase, ascorbate industrial applications. M . verticillatum could peroxidase). Hydrilla verticillata are capable of accumulate high amounts of NP and OP in their accumulating Hg effectively, though higher expo- tissues (Zhang et al. 2008a , b ). Plant also showed sures (5.0 μM) reduced chlorophyll, protein, cyste- capacity to tolerate organic chemicals such as tri- ine and NPK content. chloroacetic acid (TCA) (Hanson et al. 2002 ). Hydrilla verticillata have the capacity to absorb heavy metals Cr, Cd, Mn, Hg, Ni, Pb, Fe, 2.2.2.4 Hydrilla (Esthwaite Cu, Zn and Cr from contaminated water, thereby Waterweed) reducing pollution level of water (Samdani et al. It is native to the cool and warm waters in Asia, 2008; Shaikh and Bhosle 2011 ). Absorption Europe, Africa and Australia, with a sparse, kinetics followed Langmuir model. Ligand scattered distribution in Europe. The plant genus exchange mechanism was found to be respon- consists of one species, H . verticillata . Hydrilla sible for high Cr adsorption capacity. Both is an invasive, non-native submerged plant with roots and shoots accumulate metals such as long slender stems that branch out profusely Cu and metals are mainly accumulated in cell 36 2 Aquatic Plant Species and Removal of Contaminants

Fig. 2.4 Emergent aquatic plant species: (a ) Elodea , ( b ) Scirpus , (c ) Typha and ( d ) Phragmites wall fractions. Potential of H . verticillata for lindane degradation capacity (Ortega- Clementea bioamelioration of wastewater containing the and Luna-Pabellob 2012 ). toxic metals has been demonstrated (Gupta and Chandra 1994 , 1996 ; Rai et al. 1995 ). Exposure to high Pb and Cd reduced fresh biomass, chloro- 2.2.3 Emergent Species phyll content, protein, NR activity and glutathione levels due to toxic effect created by metals. In Typha latifolia (cattail), Phragmites (common contrast, increase in carotenoid, cysteine and reed) and Scirpus spp. (bulrush) are semiaquatic/ proline content was observed. The increase in emergent plant species that possess high metal- cysteine level under Cd stress may be due to removing abilities. Emergent plants bioconcen- enhanced levels of ATP sulfurylase and adenos- trate metals from water and sediments, though ine 5′-phosphosuphfate sulphotransferase (Singh the site where the metals are localized varies et al. 2012a ). Various Cd concentrations resulted from species to species. Most of the plants retain in the induction of phytochelatins at both con- more of the metal burden in belowground parts centrations that exhibited positive thiol reactions. (roots), in contrast to a few other species that H . verticillata has a cellular mechanism for Pb redistribute a greater proportion in aboveground detoxifi cation (Gupta et al. 1995 ; Tripathi et al. tissues, especially leaves. The metal uptake by 1996 ). plants results in the transport of metals across the plasma membrane of root cells, xylem loading Organic Contaminants and translocation, and detoxifi cation and seques- Hydrilla verticillata showed capacity for accu- tration of metals at cellular level (Fig. 2.4 ). mulation and hence removal of hydrophobic organochlorine contaminants such as cis- and 2.2.3.1 Elodea (Waterweed) trans-chlordane, dieldrin and polychlorinated It is a herbaceous freshwater plant. It is commonly biphenyls (PCBs) and hexachlorocyclohexane reported in parts of Europe , Australia , Africa , Asia (HCH), an organochloride insecticide (Hopple and New Zealand . Elodea canadensis (American and Foster 1996 ; Sinha 2002 ). HCH toxicity was or Canadian waterweed) is the most common reduced in plants treated with high Fe concentra- species. It is a rooted multi-branched perennial tions, though HCH accumulation was reduced plant. The dark-green blade- like leaves (3/5-in. in presence of high Fe. HCH exposure reduced long and 1/5-in. wide) are in whorls of three with chlorophyll content, but increased malonaldehyde fi nely toothed margins. It lives entirely underwa- content, cysteine level, thiol content and activity ter with the exception of small white fl owers of antioxidative enzymes such as superoxide dis- which bloom at the surface and are attached to mutase (SOD) (Sinha 2002 ). The plant showed the plant by delicate stalks. 2.2 Major Plant Species 37

Inorganic Contaminants Elodea canadensis removed or transformed Elodea canadensis (Elodea) showed capacity DDT from the medium. The decay profi le of for removing Fe, Cu, Zn, Cd, Pb and Ni from DDT from the aqueous culture medium followed wastewater and storm water (Fritioff et al. 2005 ; fi rst-order kinetics (Olette et al. 2008 ). DDT was Begum and HariKrishna 2010 ; Hansen et al. degraded or bound to the elodea plant material. 2011 ; Matamoros et al. 2012 ). Elodea canaden- o,p′-DDD and p,p′-DDD are the major metabolites sis also showed possibility of cleaning U from in these plants (Gao et al. 2000a , b ). Apparently, contaminated waters. E . nuttallii showed Fe reduction of the aliphatic chlorine atoms of DDT accumulation (Pratas et al. 2010). Growth of E . is the major pathway for this transformation. nuttallii was promoted by low iron concentra- It also showed capacity to remove explosives tion, but growth inhibition was observed on 2,4,6-trinitrotoluene (TNT) and hexahydro- 1,3,5- exposure to high concentration (beyond 10 mg trinitro-1,3,5-triazine (RDX) in groundwater L −1). The synthesis of protein, pigments, PSII using constructed wetlands at Milan Army maximal quantum yield, electron transport rate Ammunition Plant. It was demonstrated that and activities of antioxidant enzymes, namely, TNT disappeared completely from groundwater superoxide dismutase (SOD), catalase (CAT), incubated with plants. Emergent plants reduced peroxidase (POD) and glutathione S-transferase in groundwater amended to contain RDX. (GST) increased at low concentrations of Fe, Pb, Highest specifi c RDX removal rates were found while high concentration inhibited the synthesis in submersed plants in elodea and in emergent of protein and pigments as well as activities of plants in reed canary grass (Best et al. 1999b ). antioxidative enzymes (Dogan et al. 2009 ; Xing et al. 2010 ; Sun et al. 2011 ). Induction of non- 2.2.3.2 Typha (Cattail) protein thiol (SH) groups and ascorbate sug- It is a cosmopolitan species found in variety of gested their role in metal detoxifi cation. Cd wetland habitats in North America, Mexico, Great induced the production of phytochelatins (PCs) Britain, Eurasia, India, Africa, New Zealand and in E . canadensis . PCs were produced in a con- Australia. It is a genus of about 11 species of centration and species dependent manner (Sun monocotyledonous fl owering plants in the family et al. 2011 ). Typhaceae. Leaves are alternate and mostly basal Elodea nuttallii absorbed phosphorus via both to a simple stem that bears the fl owering spikes. roots and shoots in eutrophic lakes. The phospho- Plants are monoecious and bear unisexual, wind- rus uptake via shoots signifi cantly exceeded pollinated fl owers, developing in dense spikes . the phosphorus uptake via roots. The absorbed phosphorus was equally translocated via acripe- Inorganic Contaminants tal or basipetal movements and was incorporated Typha latifolia exhibited Zn, Pb, As and Cd tolerance in all parts of the plants (Susanne and Hendrik and exclusion potential (Ye et al. 2001 ; Abdel- 2008 ; Wang et al. 2010 ). Ghani et al. 2009; Alonso-Castro et al. 2009 ; Adhikari et al. 2010 ; Hadad et al. 2010; Hegazy Organic Contaminants et al. 2011 ). Plant removed Cd and Pb effectively E . canadensis showed uptake and elimination from solutions and was able to accumulate these capacity for microcontaminants in wetland metals in the roots and, to a lesser extent, in the systems through biodegradation and uptake pro- leaves. This may be related to its oxygen trans- cesses. This includes pesticides such as copper port capability, radial oxygen loss from the roots sulphate (fungicide), fl azasulfuron (herbicide), and the capability to modify its rhizosphere. and dimethomorph (fungicide), diclofenac, tric- Plants showed presence of inorganic arsenite, losan, naproxen, ibuprofen, caffeine, clofi bric arsenate, dimethylarsinic acid and monomethyl- acid and MCPA. The fi ndings suggested that most arsonic acid. Plaque (Fe and Mn) affected Cu of these contaminants are removed predomi- accumulation in Typha latifolia L. (Ye et al. nantly by biodegradation. 2001 ; Saulais et al. 2011 ). Plants adsorbed more 38 2 Aquatic Plant Species and Removal of Contaminants

Cu and a higher proportion of Cu was observed levels of BOD and total dissolved solids (TDS) in roots. Typha domingensis leaf powder showed and lower concentration of heavy metals such removal of Al, Fe, Zn and Pb from aqueous solu- as Pb, Mn, Zn and Cu and higher level of dis- tion. The infrared spectra of Typha leaf powder solved oxygen (DO) were noticed in the reed (Typha confi rmed ions–biomass interactions responsible angustata) root zone compared to non-reed for sorption. FTIR investigation revealed that root zone. The numbers of colonies of bacterial metal binding takes place on the surface of Typha species and fungal populations were found to biomass. X-ray fl uorescence (XRF) spectroscopy increase in reed zone than non-reed root zone. and micro-proton-induced X-ray emission Rhizosphere of Typha angustata has a direct (micro-PIXE) depicted that Pb accumulated in infl uence on the composition and density of soil root cells around vacuoles and slowly get trans- microbial community. Exudates of reed plant ported to leaves (T . angustifolia and T . latifoli a). caused an increase in the metabolic activity of Lead was deposited in the rhizome near the cell microbes of the rhizosphere and transformed the wall. Most of the Pb accumulated in leaf cells, organic and inorganic pollutants into harmless especially in chloroplasts, and vacuoles (Abdel- compounds. It is concluded that Typha root zone Ghani et al. 2009 ; Sharain-Liew et al. 2011 ). with its myriad of microbes served as a bio-bed However, in the rhizome and leaf, lead granules which has the potential to reduce the BOD and accumulated near the cell wall and in the chloro- TDS levels of sewage water, decrease the con- plasts. Increase in K, Ca, Fe and Zn concentra- centration of heavy metals and increase dissolved tion in roots, rhizomes and leaves was noted at oxygen. Typha domingensis also showed phytore- higher Pb treatments. Micro-PIXE analysis mediation of heavy metals from urban domestic demonstrated Pb accumulation and localization and municipal wastewater. The concentrations in in epidermal and cortical tissues of treated roots the root and shoot tissues were found in the order and rhizomes (Panich-pat et al. 2005 ). Cell wall of Fe > Mn > Zn > Ni > Cd. Small- scale wetland immobilization of Pb is one of the tolerance mesocosms vegetated with Typha showed effi - mechanisms in Typha latifolia (Gallardo-W illiams cacy for treatment of wastewater as signifi cant et al. 2002; Panich-pat et al. 2005 ; Ramamoorthy reduction in total suspended solids (TSS), 5-day and Kalaivani 2011 ). Results indicate that Pb may biochemical oxygen demand (BOD5) and total form complexes with phosphorus and sulphur Kjeldahl nitrogen (TKN) was noted (Calheiros compounds in roots and rhizomes, which may et al. 2009 ; Borkar and Mahatme 2011 ; Mojiri also represent attraction sites for binding Zn. 2012 ). Typha domingensis also showed capacity Higher doses of Pb altered rate of photosynthesis, to absorb and accumulate Al, Fe, Zn and Pb from chlorophyll content and POD and SOD activities industrial wastewater ponds in El-Sadat City, in Typha plants. Egypt. Maximum metal removal was achieved by Wetlands planted with Typha domingensis rhizofi ltration. could treat effl uent from metallurgical opera- The wetland microcosms signifi cantly reduced tions. The root and stele cross-sectional areas, the concentrations of Se, As, B and cyanide (CN) number of vessels and biomass registered in inlet in the wastewater. The primary sink for the reten- plants promoted the uptake, transport and accu- tion of contaminants within the microcosms was mulation of contaminants Cr, Ni, Zn and total the sediment, which accounted for 40–50 % phosphorus in tissues. The modifi cations recorded removal, while accumulation in plant tissues accounted for the adaptability of T . domingensis accounted for only 2–4 % and while 3 % of the to the conditions prevailing in the constructed Se was removed by biological volatilization to wetland, which allowed this plant to become the the atmosphere. Cattail, Thalia and rabbitfoot dominant species and enabled the wetland to grass were highly tolerant of the contaminants maintain a high contaminant retention capacity and exhibited no growth retardation. The data (Aslam et al. 2010 ). Typha angustata showed from the wetland microcosms support the view capacity to treat domestic sewage. The lower that constructed wetlands could be used to suc- 2.2 Major Plant Species 39 cessfully reduce the toxicity of aqueous effl uent with Cd exposure did not affect root and shoot contaminated with extremely high concentra- growth and mineral composition (N, P, K, Fe, Zn tions of SeCN_ , As and B, but pilot-scale studies and Mn), while combined treatments of Cd, Cu need to be carried out to validate the results and Zn signifi cantly decreased shoot length, root (Manios et al. 2003 ; Lu et al. 2009 ). number, plant fresh weight and tissue concentrations of N, P and K. Pilot subsurface horizontal Organic Contaminants flow constructed wetland with Phragmites Horizontal subsurface fl ow CWs planted with australis and Phragmites mauritianus showed Phragmites australis (UP series) and Typha domestic wastewater treatment by reducing BOD, latifolia provided high removal of organics BOD COD, suspended solids, TDS, conductivity, nitrate and COD (80–90 %) from tannery wastewater nitrogen, total phosphorus (TP) and total nitrogen and other contaminants, such as nitrogen. The (TN) (Alia et al. 2004 ; Todorovics et al. 2005 ; plant also showed capacity to remove parathion, Yang et al. 2007 ; Chale 2012 ). The results trichloroethylene, pesticide residues and pharma- obtained show that P . mauritianus may not be a ceuticals such as ibuprofen and clofi bric acid suitable plant for use in constructed wetlands (Wilson et al. 2000 ; Bankstona et al. 2002 ; (Weis and Weis 2004 ) since it sheds a lot of litter Amaya-Chávez et al. 2006 ; Dordio et al. 2007 , which introduces nutrients into the system. 2009 , 2011 ). Cattails also showed potential for Phragmites communis demonstrates an effi cient decolorizing and remediating textile wastewater approach to remove various liquid-phase pollut-

(Nilratnisakorn et al. 2009 ). ants such as Zn, COD, colour and NH3 –N from wastewater by using both free water surface 2.2.3.3 Phragmites (Reed) fl ow and submerged surface fl ow constructed It is a large perennial grass found in wetlands wetland (CW) systems (Weis and Weis 2004 ). throughout temperate and tropical regions of the Growth of Phragmites communis enables well- world. Phragmites australis is sometimes developed root network in CW system, thus leading regarded as the sole species of the genus, though to a higher adsorption capacity. The presence of some botanists divide Phragmites australis into bio-membrane on the plant root not only enhances three or four species: Phragmites australis but also stabilizes the effi ciencies for removing (Cav.) Trin . ex Steud ., Phragmites communis various contaminations from the wastewater. In a Trin., Arundo phragmites L. (the basionym ) and similar study, subsurface horizontal fl ow con- Phragmites altissimus. The perennial has alter- structed wetlands receiving tannery wastewater nately spaced spear-shaped leaves, rootstalks, vegetated with Typha latifolia and Phragmites called rhizomes and fl owers, and spikelets with australis showed reduced organic load by decreas- tufts of silky hair. ing COD and BOD (Calheiros et al. 2007 ; Kalipci Reed bed systems showed stable removal 2011 ; Ong et al. 2011 ; Cortes- Esquive et al. 2012 ; effi cacy of organics of a similar rate to the con- Ramprasad 2012 ). ventional technologies and also have higher ability of removing nutrients, so benefi cial against Organic Contaminants eutrophication. Constructed wetland planted with Phragmites australis treated azo dye Acid Orange 7 (AO7). Inorganic Contaminants Toxic signs were observed at the Phragmites aus- Phragmites australis is effective for removing tralis after the addition of AO7 into the wetland heavy metals from the industrial wastewater reactors, but it adapted to the wastewater with under arid and semi-arid conditions. Hg and As passage of time. The presence of Phragmites accumulations in belowground tissues were australis had a signifi cant impact on the removal higher than those for the aboveground tissues of organic matters, AO7, aromatic amines and

(Afrous et al. 2011 ). Hydroponic experiments NH4 –N (Davies et al. 2005 ). 40 2 Aquatic Plant Species and Removal of Contaminants

2.2.3.4 Scirpus (Bulrush) An engineered treatment wetland with E2, and The genus has a cosmopolitan distribution. It EE2 showed that 36 % of the E2 and 41 % of belongs to family Cyperaceae. Many species are the EE2 were removed during the cell’s 84-h common in wetlands and can produce dense hydraulic retention time (HRT). The attenuation stands of vegetation, along rivers, coastal deltas was most likely the result of sorption to hydro- and ponds. It is a perennial herb with short, tough phobic surfaces in the wetland coupled with rhizomes, forming dense tussocks ~2-m tall. Most biotransformation. Sorption was indicated by species have leaves reduced to tiny sheathing the retardation of the hormones relative to the structures. The fl owers or infl orescences of these conservative tracer (Gray and Sedlak 2005 ). plants are found on the tip of the growing stems Biotransformation was indicated by elevated and resemble tight clusters of grass-like fl owers. concentrations of the E2 metabolite, estrone. It was also suggested that removal effi ciency can Inorganic Contaminants be increased by increasing HRT or the density of Effi cacy of small-scale wetland mesocosms plant materials. Scirpus mucronatus showed planted with vegetation (a mixture of Typha , growth in diesel fuel- contaminated soil and could Scirpus and Juncus species) showed effi cacy for survive high concentrations of hydrocarbons. treatment of domestic wastewater by reducing 33.3 % of plants were withered in 5 and 10 g kg−1 , total suspended solids (TSS), BOD, total Kjeldahl 66.6 % on 15, 20, and 50 g kg −1, 100 % withered nitrogen (TKN) and conductivity. Increased DO on 100 and 200 g kg −1 of contaminant concentration and reduction in faecal coliform, Enterococcus , after 30 days of exposure (Purwanti et al. 2012 ). Salmonella , Shigella , Yersinia and coliphage populations also were observed in vegetated wetlands (Hench et al. 2003 ). Horizontal sub- 2.2.4 Other Plant Species surface fl ow constructed wetland planted with Limnocharis fl ava and Scirpus atrovirens showed Ipomoea aquatica (water spinach) showed effi cacy for removing nutrients (NH3 –N and capacity to grow in Cd-contaminated surface

PO4 –P) from landfi ll leachate (Kamarudzaman water and remediate Cd-contaminated wastewa- et al. 2011 ). Phragmites australis , Typha latifolia ter. Root length and root biomass were negatively and Scirpus also showed capacity for uptake of correlated with the total soluble Cd ions. High As and Hg from industrial wastewater. Higher Cd bioconcentration factors of I . aquatica (375– metal accumulation was noted in belowground 2,227 L kg −1 for roots, 45–144 L kg −1 for shoots) tissues. Lab-scale horizontal subsurface fl ow con- imply that it is a potential aquatic plant to structed wetland (CW) planted with Phragmites remediate Cd-contaminated wastewater (Wang et al. australis and Scirpus maritimus treated moderate 2008 ). Lotus (Nelumbo nucifera ) showed the best strength wastewater (Afrous et al. 2011 ). The removal effi ciency for wastewater (domestic) physicochemical characteristics of the wastewater treatment. Plant showed removal of SS, BOD5, changed signifi cantly as the wastewater fl owed TKN, NH3 –N, NO2 –N, NO 3 –N, TP and coliform through the respective wetland cells. CW unit bacteria (Kanabkaew and Puetpaiboon 2004 ). with zeolite achieved signifi cantly higher removal Vetiveria zizanioides (vetiver grass) showed for COD, ammonium, TSS and total nitrogen at capacity to tolerate very high levels of heavy 4- and 3-day HRT (Gross et al. 2007 ; Shuib et al. metals Al, Mn, Mg, As, Cd, Cr, Ni, Cu, Pb, Hg, 2011 ; Sharif et al. 2013 ). Se, Zn and the herbicides and pesticides in soils and water. It could also resist very high acidity, Organic Contaminants alkalinity and salinity conditions (pH from 3.0 Estrogenic hormones 17b-estradiol (E2) and to 10.5; EC = 8 dScm). Vetiver also has high capac- 17a-ethinyl estradiol (EE2) have been detected ity to absorb and remove agro-chemicals like in municipal wastewater effl uent and surface carbofuran, monocrotophos and anachlor from waters at concentrations toxic to aquatic fauna. soil, thus preventing them from contaminating and Literature Cited 41 accumulating in the crop plants. It also showed Al-Baldawi IA, Abdullah SRS, Suja F, Anuar N, Idris M an ability to tolerate very high acidity, alkalinity (2012) Preliminary test of hydrocarbon exposure on Azolla pinnata in phytoremediation process. In: (pH from 3.0 to 10.5); soil salinity (EC = 8 dScm), International conference on environment, Energy and sodicity (ESP = 33 %), magnesium and very high biotechnology IPCBEE, vol 33. 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Ceratophyllum demersum L. Environ Sci Pollut Res Zayed A, Pilon-Smits E, de Souza M, Lin ZQ, Terry N Int 19:3969–3976 (2000) Remediation of selenium polluted soils and Yadav SB, Jadhav AS, Chonde SG, Raut PD (2011) waters by phytovolatilization. In: Terry N, Barnuelos Performance evaluation of surface fl ow constructed G (eds) Phytoremediation of contaminated soil and wetland system by using Eichhornia crassipes for water. Lewis, Boca Raton, p 61 wastewater treatment in an institutional complex. Univ Zhang X, Lin AJ, Zhao FJ, Xu GZ, Duan GL, Zhu YG J Environ Res Technol 1:435–444 (2008a) Arsenic accumulation by the aquatic fern Yang Q, Chen ZH, Zhao JG, Gu BH (2007) Contaminant Azolla : comparison of arsenate uptake, speciation and removal of domestic wastewater by constructed wet- effl ux by Azolla caroliniana and Azolla fi liculoides . lands: effects of plant species. J Integr Plant Biol Environ Pollut 156:1149–1155 49(4):437–446 Zhang Z, Wu Z, Li H (2008b) The accumulation of alkyl- Ye ZH, Baker AJM, Wong MH, Willis AJ (1997) Zinc, phenols in submersed plants in spring in urban lake, lead and cadmium tolerance, uptake and accumulation China. Chemosphere 73:859–863 by Typha latifolia . New Phytol 136:469 Zhang X, Hu Y, Liu Y, Chen B (2011) Arsenic uptake, Ye ZH, Cheung KC, Wong MH (2001) Copper accumulation and phytofi ltration by duckweed uptake in Typha latifolia as affected by iron and ( Spirodela polyrhiza L.). J Environ Sci (China) manganese plaque on the root surface. Can J Bot 23(4):601–606 79:314–320 Zhu YL, Zayed AM, Qian JH, Souza M, Terry N (1999) Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation Phytoaccumulation of trace elements by wetland of trace elements by wetland plants, I: Duckweed. plants. II water hyacinth (Eichhornia crassipes ). J Environ Qual 27:715 J Environ Qual 28:339 Mechanism of Removal of Contaminants by Aquatic Plants 3

Plants possess highly specifi c and effi cient their transport and entrance into the vascular mechanisms to acquire essential micronutrients cylinder. Contaminants move through epidermis, from the environment. Uptake and removal of Casparian strip and endodermis from where they contaminant varies for each category of aquatic are sorbed, bound or metabolized (Shimp et al. macrophyte i.e. free-fl oating, submerged and 1993 ). The organic–metal complex (soluble, less emergent. The mode of uptake by plants is also toxic) is transported to cell compartments with different for organic and inorganic contaminant. low metabolic activity, i.e. cell wall and vacuole, Uptake of inorganic compounds (ionic or com- where it is stored in the form of a stable organic plexed form) is mediated by active or passive or inorganic compound. Extraordinary high lev- uptake mechanisms within the plant, whereas els of contaminants (thousands of ppm) taken up uptake of organic compounds is generally gov- from the environment are generally concentrated erned by hydrophobicity (log k ow ) and polarity. in roots, shoots and/or leaves. Uptake, transport Uptake of pollutants by plant roots is different for and storage mechanism vary for each category of organic and inorganic compounds. Uptake of contaminant removed by aquatic plants. inorganic contaminants is facilitated by membrane transporters, while uptake of organic contaminants is driven by simple diffusion based on 3.1.1 Heavy Metals their chemical properties. Assimilated and absorbed contaminant is then transformed and Aquatic plants accumulate/remove metals and detoxifi ed by a variety of biochemical reactions other toxic elements from water by phytosorption in the plant system using versatile enzymatic phytofi ltration, phytostabilization and phytoex- machineries. traction mechanisms (Tangahu et al. 2011 ). The metal bioremoval in aquatic plants include: 3.1 Inorganic Contaminants (a) Bioaccumulation—A slow, irreversible ion sequestration process. It is a passive process Uptake of inorganic contaminants, mainly nutri- of metal uptake and primarily involves adsorp- ents, heavy metals and radionuclides in aquatic tion when plants are in direct contact with the plants, takes place by roots and foliar absorption. medium and results in the accumulation of The primary role of roots is expected to be nutri- metals mainly in aerial parts of the plants. ent assimilation, and the main role of foliage (b) Biosorption—An initial, fast, reversible is inorganic carbon fi xation. In fl oating macro- metal-binding process. The active (rapid) phytes, uptake takes place predominantly by uptake of metal occurs mainly by roots from foliar absorption only. The uptake is followed by where it is translocated to other plant parts.

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 51 DOI 10.1007/978-81-322-1307-9_3, © Springer India 2013 52 3 Mechanism of Removal of Contaminants by Aquatic Plants

Phytodegradation Volatilization Metabolism Transpiration leaves Sequestration (vacuole) Translocation (xylem) stem

Phytostabilization Rhizodegradation (rhizosphere)

Uptake

roots

Fig. 3.1 Possible mechanisms of contaminant removal by plants

Removal of metal ions occurs via interactions metal burden in below-ground parts (roots), in with functional groups that are found in the pro- contrast to a few other species that redistribute a teins, lipids and carbohydrates present in the cell greater proportion in above-ground tissues, espe- walls. The kinetics for metal adsorption by aquatic cially leaves (Dhir 2010 ). The removal of metal plants fi t well in Langmuir and Freundlich iso- from water depends on factors such as: therms and follows fi rst-order kinetics (Fig . 3.1 ). • Sediment geochemistry In free-fl oating aquatic plant species, the • Water physico-chemistry active (rapid) uptake of metal occurs mainly by • Plant physiology roots, from where it is translocated to other plant • Plant genotype parts. In submerged plant species, leaves are the The metal uptake in emergent plants is facili- main site of mineral uptake. The foliar absorption tated by specialized structures called metal-rich of heavy metals occurs by passive movement rhizoconcretions or iron plaque present on root through the cuticle, where the negative charges of surface. These structures are mainly composed of the pectin and cutin polymers of the thin cuticle iron hydroxides and metal such as Mn that are and polygalacturonic acids of the cell walls cre- immobilized and precipitated on root surface. ate a suck inward (Dhir 2010 ). Due to an increase Plaque restricts metal uptake at low pH but facili- in charge density inward, the transport of positive tates uptake at higher pH. The anaerobic environ- metal ions takes place. ment in bottom water and sediments promote The mechanism of metal removal in sub- metal uptake as metals are present in more solu- merged plants involves: ble less oxidized forms. • Passive penetration of ions in apparent free The rate of absorption, accumulation and space (AFS) translocation of metal in plants depends on plant • Active uptake of ions into cytoplasm species and is further regulated by environmental • Active storage of ions into vacuoles from the factors like temperature, pH, redox potential, cytoplasm time, dose, temperature, agitation speed and Emergent plants absorb, translocate and bio- salinity. The rate of heavy metal removal is con- concentrate metals from water and sediments. centration and time dependent. pH regulates the Most of the metal is immobilized in soils in availability of metals to macrophytes through rhizosphere zone from where it is reduced to sul- speciation of metals. The redox potential also phite or metallic form. Most of the plants retain regulates heavy metal uptake in plants. Low 3.1 Inorganic Contaminants 53 redox potential supports the metal binding to species. Uptake of inorganic ions is saturable sulphides in sediments, thus immobilizing them. following Michaelis–Menten kinetics Salinity decreases the uptake of metals in plants (Marschner 1995 ). due to the formation of chloride complexes. (c) Storage Chelators such as siderophores, organic acids The translocation is followed by compart- and phenolics released by plants, and bacteria mentalization, i.e. metal deposition in vacu- enhance bioavailability of metals and hence oles driven by ATP-dependent Cd/H+ antiport promoting uptake. or ABC proteins or excretion by specifi c The metal uptake by plants results in accumu- glands. The metal toxicity in plants induces lation in the root itself or their transport (translo- oxidative stress that induces alterations in cation) across the plasma membrane of root cells, membrane structures. This is curtailed by xylem loading, detoxifi cation and sequestration various tolerance mechanisms that include: of metals at cellular level. The heavy metals are • Chelation binding of metal ions by high- incorporated in plant tissues or stored in bound affi nity ligands, which reduce the concen- form. Uptake–translocation mechanisms are tration of free metal ions in the solution. likely to be closely regulated. In general, the These mainly include binding of metal heavy metal removal mechanisms in plants ions via thiol-rich peptides such as phyto- include three steps: uptake, translocation and chelatin (PC) and metallothionein (MT) storage. synthesis, amino acids and organic acids. (a) Uptake Phytochelatins (PC) have high affi nity for Plant roots solubilize and take up micro- binding heavy metals such as Cd, Hg, Cu nutrients from very low ppb levels to very or As. high ppm levels in the soil. Ion uptake is • Synthesis of stress metabolites and/or facilitated by (1) proton pumps such as proteins. ATPases, (2) co- and antitransporters and • Effi cient antioxidant machinery. (3) channels. Uptake effi ciency depends on • Biotransformation, the toxicity of the physicochemical properties of the contami- metal can be reduced by plants by the nant, chemical speciation and the plant’s chemical reduction of the element and/or capacity. Inorganic contaminants are taken incorporation into organic compounds or up predominantly via membrane transporter enzymatic degradation. proteins. Arsenic (as arsenate) might be • Reduced uptake or effl ux pumping of taken up by plants due to the similarities to metals at plasma membrane. the plant nutrient phosphate, while Se • Binding to cell wall. replaces the nutrient sulphur in compounds • Cytoplasmic Ni seems to be detoxifi ed by taken up by a plant (Brooks 1998 ; Abedin binding to histidine, while vacuolar stor- et al. 2002 ). age of Ni is probably in the form of citrate (b) Translocation (Dhir et al. 2009 ) . Metal transport is assisted by specialized Strong chelators effi ciently bind the metals in proteins embedded in the plant cell plasma a non-toxic form, thereby allowing fl ux through membrane. Transport proteins besides facili- the xylem up to the leaves. The metal hyperac- tating metal uptake in plants also play an cumulator contains constitutively high organic important role in homeostasis. Some of these acid and phenolic levels, which form strong com- proteins include ATPases, Nramps, cation plexes with the metal thus maintaining cation/ diffusion facilitator (CDF) proteins and zinc anion homeostasis. According to malate shuttle ion permeases (ZIP). Cation diffusion faci- hypothesis, in Zn-resistant plants, excess Zn is litators (CDF type), the ABC transporters bound to malate in the cytoplasm, and after for phytochelatins and the metal chaperones transport to the vacuole, a ligand exchange are commonly reported in hyperaccumulator occurs. Zn forms more stable complexes with 54 3 Mechanism of Removal of Contaminants by Aquatic Plants citrate, oxalate or other ligands, while malate refl ecting a higher demand for GSH under As returns to the cytoplasm. stress. The PC–arsenite complexes are likely Heavy metal toxicity increases cellular reac- to be stored in vacuoles. ATP-binding cassette tive oxygen species, such as superoxide anion, (ABC) proteins confer arsenite resistance by hydroxyl anion and hydrogen peroxide which transporting the glutathione S -conjugated arse- causes oxidative stress. The reactive oxygen spe- nite into the vacuole. The PC-arsenite com- cies are deactivated by enzymatic (superoxide plexes are also likely to be transported into dismutase, catalase, ascorbate peroxidase, guaia- vacuoles by an ABC protein (Zhao et al. 2010 ) . col peroxidase and glutathione reductase) and nonenzymatic (glutathione, ascorbic acid, phenolic compounds and tocopherol) antioxidant sys- 3.1.2 Radionuclides tems (Parvaiz et al. 2008 ; Azqueta et al. 2009 ). The mechanism of uptake and transport for Aquatic plant species exhibit an equally high some heavy metals such as As has been studied in potential to accumulate radionuclides. The detail. uptake and reduction of radionuclides by aquatic 1. Uptake plants is rapid as they are actively transported Arsenate, arsenite, monomethylarsonic across the plasma membrane. In aquatic plants, acid (MMA) and dimethylarsinic acid (DMA) the major mode of entrance of radionuclides is are the common forms of As present in soil foliar absorption where it is photoreduced (chlo- available for plant uptake. Plant roots take up roplast), followed by complexation with ligands arsenite mainly as the neutral molecule present in the cell including proteins, cysteine

As(OH)3 . Arsenate is taken up phosphate and glutathione. Kinetic studies indicate that transporters. Arsenate is taken up by plant radionuclide absorption by plants is time and roots via phosphate transporters and reduced concentration dependent and depicts ﬁ rst-order to arsenite in root cells. uptake rate (Popa et al. 2006 ; Dhir et al. 2009 ). 2. Transport In general, the uptake of radionuclides in In higher plants, arsenite, methylated As, plants involves two steps: enters plant root cells via nodulin 26-like 1 . Passive : a rapid binding of ions to negatively intrinsic proteins (NIPs) that are the structural charged groups on the cell surface and trans- and functional equivalents of the microbial port through the cell wall within a short and mammalian aquaglyceroporins (Wallace duration et al. 2006 ). NIPs are a subfamily of the plant 2 . Active : metabolically dependent penetration major intrinsic proteins (MIPs), collectively of ions through cell membrane, movement known as aquaporins or water channels inside cytoplasm and the bioaccumulation of (Maurel et al. 2008 ). Aquaporins also facili- the metal ions onto the protoplasts tate the transport of methylated forms. In most In aquatic plants, the major mode of entrance

plant species, arsenite is the main form loaded for Tc is foliar absorption of TcO4 −. Technetium − into the xylem sap. The dominance of triva- (TcO4 ) taken up by plants is actively transported lent As in plant tissues when arsenate is the across the plasma membrane or transported to form supplied to plants indicates a high capac- leaves, where it is photoreduced (chloroplast), fol- ity of arsenate reduction. lowed by complexation with ligands present in the 3. Storage cell including proteins, cysteine and glutathione. It is detoxifi ed by complexation with thiol- The total amount of Tc present in plants is the sum rich peptides and sequestrated in the vacuoles of both the pertechnetate and reduced Tc form in As non-hyperaccumulating plants. Arsenic (Hattink et al. 2000 , 2003 ). The fractions of poly- is a strong inducer of PC synthesis. A number saccharides and lipids present on the cell surface of genes or enzymes involved in glutathione are actively involved in the accumulation of radio- synthesis, metabolism and transport are upreg- nuclides. The uptake of radionuclides is also facili- ulated on exposure to arsenate, probably tated by the presence of carbonate groups present 3.2 Organic Contaminants 55 on the surface of the plant (Dhir et al. 2009 ). The hypothesis states that Cs infl ux occurs through mechanism of uptake and translocation of some the K channels but that the ratio of Cs to K in the radionuclides have been studied in detail. effl ux part varies with K supply. Potassium starvation induces the expression of K + transporters, 3.1.2.1 Caesium (Cs) Transport such as HKT1 (high-affi nity K+ transporter) in Plants which may increase Cs+ uptake. Uptake Caesium uptake in plants takes place through roots and is facilitated by two transport systems 3.1.3 Nitrogen and Phosphorus located on plant root cell membranes, namely, the + + + K transporter and the K channel pathway (Zhu The uptake of nitrogen in the forms of NH4 and − and Smolders 2000 ). Caesium absorption by NO3 has been reported for aquatic species plant roots is rapid and this is followed by trans- (Henriksen et al. 1992 ; Lazof et al. 1992 ; Rao location to the above-ground plant parts. Lower et al. 1993 ; Reidenbach and Horst 1997 ; Gessler K concentrations in solution promote Cs uptake. et al. 1998; Cedergreen and Madsen 2002 ). Lemna At low K concentrations, Cs+ is absorbed by the minor has shown the capacity to take up signifi - K+ uptake system of the root. Higher concentra- cant amounts of inorganic N through both roots tions of K+ strongly suppresses Cs+ uptake. Cs+ is and fronds. High nutrient uptake capabilities of effi ciently transported by high-affi nity K+ uptake leaves have also been reported for the submerged + transporter. Increasing concentrations of NH4 macrophytes Ruppia maritima and Zostera reduce uptake of Cs, while increasing concentra- marina, where weight-specifi c uptake rates of 2+ 2+ 3− + tions of divalent cations Ca and Mg slightly PO 4 and NH 4 by leaves are noted. Eichhornia reduce the uptake of Cs. This is because divalent crassipes, Salvinia auriculata, Phragmites aus- cations compete with Cs uptake through compe- tralis and Phalaris arundinacea exhibited tition in the apoplast. removal capacity for nitrogen and phosphorus

such as of NO3 −N, NH4 −N and PO4 −P (Petrucio Transport and Esteves 2000 ). The removal of nitrate nitro-

Carrier and channel modes have been proposed gen (NO3 −N) in natural and constructed wetland as possible mechanisms with a molecular basis systems occurs via three interacting processes: for the transport of K+ across cell membranes of plant uptake, microbial assimilation/immobiliza- plant roots. Carrier-mediated transport is facili- tion and denitrifi cation. Most denitrifying bacteria tated by a high-affi nity system (transporter) require anoxic conditions and a labile organic car- within cell membranes operating predominantly bon source to biologically reduce nitrate to nitro- at low external K concentration (<0.3 mM). gen gas (N2) (Zhu and Sikora 1994 ; Vymazal and Potassium is transported across the plasma mem- Kropfelova 2008 ). Nitrogen and P removal are brane against the electrochemical gradient via temperature dependent as higher removal is noted this system. This transporter (HKT1) is probably in summer than winter. Phosphorus is taken up in a K+ H+ cotransporter. It has been suggested that the form of phosphate and uptake is facilitated by multiple high-affi nity K+ transport systems may ion channels or proton pumps. be involved in K+ uptake. Channel-mediated transport is a low-affi nity system operating at high external K concentrations (above 0.5–1 mM) 3.2 Organic Contaminants (Zhu et al. 2000 ). The high-affi nity transport system follows the Michaelis–Menten equation Aquatic plant species possess the potential to (i.e. saturation kinetics) and is believed to be remove, sequester and transform organic contam- carrier- mediated (H+ cotransporter), whereas inants. The capacity of aquatic plants for uptake the low- affi nity one exhibits linear kinetics and and accumulation of organophosphorus, organo- is expected to be channel-mediated. Another chlorine compounds, and chlorobenzenes has 56 3 Mechanism of Removal of Contaminants by Aquatic Plants

been studied extensively (Gobas et al. 1991 ; Rice (c) Hydrophobicity (K ow ) et al. 1997 ; Macek et al. 2000 ). Uptake of organic (d) Volatility of the contaminant contaminants is driven by simple diffusion based (e) Molecular weight of organic compounds on their chemical properties. In order to penetrate The inherent ability of the roots to take up into a leaf, the organic contaminant should pass organic compounds depends upon hydrophobic- through the stomata or traverse the epidermis, ity (or lipophilicity) of the target compounds which is covered by ﬁ lm-like wax cuticle. The (Schnoor et al. 1995). This parameter is often majority of toxic compounds penetrate into a leaf expressed as the log of the octanol–water parti- as solutions (pesticides, liquid aerosols, etc.). tioning coefﬁ cient, K ow . Generally the higher the

Plants absorb xenobiotics primarily through roots log K ow , the greater the root uptake of compound. and leaves ( Wang and Liu 2007 ). Leaf absorption An optimum log K ow value is required for a com- is often a consequence of agricultural spraying pound to be a good candidate for phytoremedia- with organochemicals, while volatile compounds tion. Burken and Schnoor (1997 ) predicted a are taken up directly (Burken et al. 2005 ). Organic model that showed that uptake of organic pollut- pollutants pass the membrane between root ants by plants was based on log K ow . Moderately symplast and xylem apoplast via simple diffu- hydrophobic compounds (0.5 < log Kow < 4.5) sion. Entry of organic pollutants into the xylem would be signifi cantly taken up and translocated depends on similar passive movement over inside plant tissues. More hydrophobic com- membranes as their uptake into the plants pounds are more strongly bound to root surfaces (Nwoko 2010 ). Penetration into roots occurs or partition into root solids, resulting in less mainly by simple diffusion through unsuberized translocation within the plant (Cunningham et al. cell walls, from which xenobiotics reach the 1996 ). In contrast, highly soluble organic com- xylem stream. There are no specifi c transporters pounds can be readily taken up by plants. Organic in plants for these man-made compounds, so the compounds cover a wide range of polarity (log movement rate of xenobiotics into and through Dow from −2 to 6), biodegradability and photo- the plant depends largely on their physico- degradability (Calderón-Preciado et al. 2011 ; chemical properties. Murray et al. 2012 ). The passive uptake of Removal of organic contaminants involves contaminant is driven by availability of the con- two major mechanisms: taminant in its protonated form. The protonated 1. Direct uptake of contaminants followed by form of the contaminant is considered as the metabolization and subsequent accumulation species available for biotic partitioning in plants, of non-phytotoxic metabolites into the plant which further gets coupled to enzymatic transfor- tissue mation and compartmentalization in vacuoles. 2. Release of exudates and enzymes that stimu- Kinetics revealed the fi rst-order rate equations late microbial activity and the resulting for the uptake and elimination of organic contami- enhancement of microbial transformations in nants by aquatic plants. the rhizosphere (the root zone) Plant uptake of organic compounds depends The potential of aquatic plants to sequester on the type of plant, contaminant and many other organic contaminants depends upon the plants lipid physical and chemical characteristics of the soil. rich cuticle, which helps in the sequestration of A typical microbial population in the rhizosphere lipophilic organic compounds (Dhir et al. 2009 ). comprises bacteria, actinomycetes and fungi. The amount of organic compound sequestered The roots of the plants exude a wide spectrum by aquatic plants depends on: of compounds including sugars, amino acids, • The plant species carbohydrates and essential vitamins that may • Biochemical composition of the plant tissues act as growth and energy-yielding substrates • Physicochemical properties such as: for the microbial consortia in the root zone.

(a) Polarity (D ow ) Exudates may also include compounds such as (b) Aqueous solubility acetates, esters, benzene derivatives and enzymes. 3.2 Organic Contaminants 57

Plant root exudates can change metals speciation Phase I conversion/activation (i.e. form of the metal) and the uptake of metal Organic compound undergoes hydrolysis, ions and simultaneous release of protons, which reduction and oxidation. This facilitates its acidifi es the soil and promotes metal transport uptake and assimilation (Eapen et al. 2007 ; and bioavailability. Plants provide exudates that Komives and Gullner 2005). Introduction of provide an excellent habitat for increased micro- functional groups to the organic compounds bial populations and pump oxygen to roots, a results in the formation of more polar, chemi- process that ensures aerobic transformations near cally active and water-soluble compounds the root that otherwise may not occur in the bulk (Komives and Gullner 2005 ). In plants, oxidative soil. Exudates stimulate bacterial transformations metabolism is mediated mainly by cytochrome and build up the organic carbon in the rhizo- P450 monooxygenase (Sandermann 1994 ). sphere. Microbial populations present in the rhi- These enzymes are very crucial during the oxi- zosphere enhance degradation of organics by the dative process of bioactivation, to emulsify provision of appropriate benefi cial primary sub- highly hydrophobic pollutants and make them strates for co-metabolic transformations of the chemically reactive electrophilic compounds target contaminants. Enzymes such as dehaloge- which form conjugates (Morant et al. 2003 ). nase, nitroreductase, peroxidase, laccase, nitrilase and oxygenase help in signifi cant transformation Phase II conjugation of contaminants. The organic compounds in the Activated organic metabolite gets conjugated root exudates can stimulate microbial growth in or bounded with sugar, amino acids and glutathi- the rhizosphere (the region immediately sur- one or sulphydryl (–SH) group of glutathione rounding plant roots). Fungi associated with resulting in hydrophilic forms. Conjugation some plant roots (i.e. mycorrhizae) can also infl u- results in the formation of high-molecular- ence the chemical conditions within the soil. weight, more polar and less toxic compounds as Decaying roots and above-ground plant material compared to the original compound. Glutathione that is incorporated into the soil will increase the S- transferases catalyze the nucleophilic attack organic matter content of the soil, potentially of sulphur atom glutathione on electrophilic leading to increased sorption of contaminants group of variety of hydrophobic organic sub- and humifi cation (the incorporation of a com- strates. Conjugation takes place in the cytosol. pound into organic matter). Mycorrhizal fungi, Transformation of organochlorine pesticides is growing in symbiotic association with the plant, the hydroxylation of 2,4-D followed by conjuga- have unique enzymatic pathways that help to tion with glucose and malonyl and deposition degrade organics (Kvesitadze et al. 2009 ). in vacuoles . The metabolic pathways for the transforma- Every enzyme that participates in detoxifi cation of organic contaminants by aquatic plant tion process has specifi c functions (Table 3.1 ). species have been identifi ed. The exposure of Dehalogenase dehalogenates chlorinated sol- aquatic plants to organic chemicals results in: vents and is specifi cally noted in hybrid poplar (a) Rapid uptake or sequestration followed by ( Populus spp.) parrot feather (Myriophyllum (b) Transformation or degradation, either reduc- aquaticum ). Laccase cleaves aromatic ring after tive or oxidative TNT is reduced to triaminotoluene and has been (c) Assimilation of metabolites by covalent reported in stonewort (Nitella spp.) and parrot binding to plants feather (Myriophyllum aquaticum). Nitrilase Since the metabolic capacities tend to be cleaves cyanide groups from aromatic ring and enzymatically and chemically similar to those has been reported in willow ( Salix spp.). processes that occur in mammalian livers, this is Nitroreductase reported in hybrid poplar (Populus referred as ‘green livers’. The three sequential spp.) , Stonewort (Nitella spp.) and parrot feather steps/phases of the green liver model involved in ( Myriophyllum aquaticum) reduces nitro groups metabolization of organics are: on explosives and other aromatic compounds. 58 3 Mechanism of Removal of Contaminants by Aquatic Plants

Table 3.1 Enzymes participating in various processes of contaminant transformation S. no. Type of enzyme Function Step I 1. Oxidases Hydroxylation, dehydrogenation, demethylation, other oxidative reactions (cytochrome P450- containing monooxygenases, peroxidases, phenol oxidases, ascorbate oxidase, catalase) 2. Reductases Reduction of nitro groups (nitroreductase) 3. Dehalogenases Splitting atoms of halogens from halogenated and polyhalogenated xenobiotics 4. Esterases Hydrolyzing ester bonds in pesticides and other organic contaminants Step II 5. Transferases Transfers one group or moiety from one molecule to another (glutathione S -transferase (GST), glucuronozyl-O -transferase, malonyl-O -transferase, glucosyl-O -transferase) Step III 6. Transferases Transfers one group or moiety from one molecule to another (glutathione S- transferases) Others Nitrilase Cleaves cyanide groups on explosives and other aromatic compounds Peroxidase Degradation of phenols Laccase Cleaves aromatic ring after TNT is reduced to triaminotoluene Phosphatase Cleaves phosphate groups from organophosphate pesticides

Peroxidase that helps in degradation of phenols can be excreted for storage outside the plant. has been noted in horseradish (Armoracia rusti- Once an organic chemical is taken up by plant, it cana ), while phosphatase that cleaves phosphate can be transformed via lignifi cation, volatiliza- groups from organophosphate pesticides has tion, metabolization or mineralization to car- been reported in giant duckweed ( Spirodela bon dioxide, water and chlorides. Deto-xifi cation polyrhiza ) (Susarla et al. 2002 ). mechanisms may transform the parent chemical to non-phytotoxic metabolites, including lignin, Phase III, sequestration/compartmentation that are stored in various places in plant cells During compartmentation, organic com- (Coleman et al. 1997; Dietz and Schnoor pounds are conjugated and segregated into 2001 ). Cytosolic metabolites are transported to vacuoles or bound to the cell wall material (hemi- the vacuoles or apoplast by tonoplast membrane- cellulose or lignin). The sequestration of organic bound transporters. Vacuolar compartmentaliza- compounds such as halogenated organic com- tion is a major step in detoxifi cation of organics pounds by plants includes rapid physical (Coleman et al. 2002 ). ATPase is the main (adsorption, absorption, partitioning) and chemi- enzymes involved in this transport (Martinois cal processes (complexation and reaction with et al. 1993 ). Cytochrome P450, peroxygenases cuticular and membrane components). Kinetics and peroxidases are involved in plant oxidations revealed the fi rst-order rate equations for the of xenobiotics. Other enzyme classes like uptake and elimination of organic contaminants glutathione S -transferases, carboxylesterases, by aquatic plants. The potential of aquatic plants O -glucosyltransferases, O -malonyltransferases, to sequester organic contaminants depends upon N-glucosyltransferases and N-malonyltransferases the plants lipid rich cuticle, which helps in the are associated with xenobiotic metabolism in sequestration of lipophilic organic compounds. plant cells, transport of intermediates and com- The xenobiotic conjugates can also be incorpo- partmentation processes (Sandermann 1992 , rated into biopolymers such as lignin where 1994 ) (Fig. 3.2 ). they are characterized as nonextractable/bound The mechanism of removal of some organic residues, whereas in aquatic/wetland plants they contaminants has been studied in detail. 3.2 Organic Contaminants 59

CO Non-transformed 2 contaminant Insoluble conjugates in cell wall

Excretion oxidation Storage of soluble Attachment with conjugate Organic contaminant functional groups in vacuole

Conjugation with metabolites

Fig. 3.2 Fate of organic contaminant in plant cells (Modiﬁ ed from Kvesitadze et al. 2009 )

3.2.1 Halogenated Compounds dichlorodiphenyltrichloroethane (DDT) (Nzengung et al. 1999 ; Nzengung and Jeffers 2001 ). The phyto- The mechanisms involved in the removal of reduction products either get oxidized into polar halogenated organic compounds from water by compounds or are covalently bound to plant tissues aquatic plant species include: (assimilated), though the concentration of reduction • Rapid sequestration by partitioning to the products is always higher for any plant species than lipophilic plant cuticles the oxidation products. Garrison et al. ( 2000 ) • Phytoreduction to less halogenated metabo- reported enzyme-mediated reductive transforma- lites and phytooxidation tion processes in plants. A dehalogenase activity • Assimilation into plant tissues as non-toxic from Elodea that reductively transformed HCA to products, presumably formed by covalent form perchloroethylene (PCE) is also reported. binding with the plant tissues Studies with Elodea also established the reduction The sequestration of organic compounds such as of DDT to corresponding DDD analogs, plant- halogenated organic compounds by plants includes bound fractions and other unknown products (Gao rapid physical (adsorption, absorption, partitioning) et al. 2000a , b ). Another plant-derived enzyme, and chemical processes such as complexation and dehalogenase, helps reduce chlorinated solvents reaction with cuticular and membrane components. such as trichloroethylene (TCE) to chloride ion, Absorbed contaminant is transformed by a variety carbon dioxide and water. of biochemical reactions and versatile enzymatic A dehalogenase activity from Elodea reduc- machineries in the plant system. Phytoreduction tively transformed hexachloroethane (HCA) to reactions in plants are catalyzed by enzymes like form perchloroethylene (PCE). Studies with dehalogenases, such as glutathione S-transferase Elodea also established the reduction of DDT to and Fe–S clusters in chloroplast ferredoxin, while corresponding DDD analogs, plant-bound frac- phytooxidation and covalent binding (phyto- tions and other unknown products. assimilation process) are reactions mediated by oxidative enzymes (possibly cytochrome P450 3.2.1.1 Polychlorinated Biphenyls with monooxygenase activity, glutathione or (PCBs) laccase). The phytoreduction reactions mainly PCBs are xenobiotic chlorinated aromatic com- include dehalogenation reactions, which have pounds categorized as persistent organic pollut- been reported speciﬁ cally for halogenated com- ants (POPs) detected in virtually every pounds such as hexachloroethane (HCA) and compartment of the ecosystem, including air, 60 3 Mechanism of Removal of Contaminants by Aquatic Plants

water, soil, sediment and living organics. PCBs fast with the degree of chlorination. At low log K ow , are highly hydrophobic, leading to their bioaccu- higher-chlorinated compounds would not be taken mulation in living organisms (biomagnifi cation). up inside plant tissues, mono- to tetrachlorinated Processes involved in phytoremediation of PCBs PCBs can be adsorbed to plant roots, but only include rhizoremediation, phytoextraction and lower-chlorinated PCBs were translocated to phytotransformation. Due to their high hydro- aerial parts (mono-, di- and trichlorinated PCBs phobicity, PCBs bind strongly to soil particles to upper stems and mono- and dichlorinated and are only poorly taken up inside plant tissues PCBs to shoots) (Van Aken et al. 2010 ). (Aken et al. 2010 ; Das and Chandran 2011 ). Therefore, microbes in the rhizosphere play a Metabolism dominant role in their biodegradation. There are Metabolism of PCBs varies according to the many processes by which vegetation can stimu- plant species and degree of chlorination and late microbial activity in soil and enhance bio- substitution pattern. Metabolism of xenobiotic degradation of recalcitrant PCBs: compounds including PCB is a three-phase (a) Plant roots release organic compounds, process. Phase I involves oxidation of PCBs to such as sugar, amino acids and organic produce various hydroxylated products, charac- acids, that can be used as electron donors to terized by a higher solubility and reactivity. This support aerobic co-metabolism or anaero- step serves to increase water solubility and pro- bic dehalogenation of chlorinated com- vides an opportunity for conjugation via glyco- pounds. In some instances, microbial aerobic sidic bond formation. Phase II involves metabolism consumes oxygen, resulting conjugation of activated compounds with mol- in anaerobic conditions favourable to PCB ecules of plant origin (e.g. glutathione or amino dehalogenation. acids) forming adducts less toxic and more sol- (b) Plants secrete extracellular enzymes that can uble than parent PCBs. Phase III involves initiate transformation of PCBs and facilitate sequestration of the conjugates in plant organ- further microbial metabolism. elles (e.g. vacuole) or incorporation into plant (c) Plants release inducers that enhance micro- structures (e.g. cell wall). bial degradation. Plant phenolic exudates enhance the activity of the PCB degrader, B. Transformation xenovorans LB400. Metabolism of PCBs in plants involves enzyme (d) Plants increase soil permeability and oxygen oxygenases including cytochrome P450 mono- diffusion in the rhizosphere, which poten- oxygenases and peroxidases. Studies suggest the tially enhances microbial oxidative transfor- role of three enzymes including peroxidases, mation by oxygenases. Remazol Brilliant Blue R (RBBR) oxidases and (e) Plant roots are also known to secrete diverse cytochrome P450s in PCB metabolism in plants microbial growth factors. (Aken et al. 2010). Conjugative enzymes involved (f) Plant roots release organic acids and molecules in PCB metabolism involve the role of various that can act as surfactants, therefore mobilizing transferases, such as glutathione S -transferases PCBs and rendering them more susceptible to (e.g. conjugation of glutathione with several be absorbed inside plant tissues. pesticides) and glycosyltransferases (e.g. conju- (g) Plant root exudates, including phenolic com- gation of glucose with chlorophenols and DDT). pounds, fl avonoids and terpenes, increase These are likely to be involved in the conjugation microbial activity in soil and hence biodegra- and compartmentation of PCB adducts in plant dation of PCBs. tissues. Plant tolerance to several chlorinated pollutants, such as atrazine, metolachlor and 1-chloro- Uptake 2,4-dinitrobenzene (CDNB), can be enhanced The effi ciency of plant uptake of PCBs—with log by the overexpression of enzymes involved in

K ow ranging from 4.5 (2-monochlorobiphenyl) to glutathione synthesis, including γ-glutamylcysteine 8.2 (decachlorobiphenyl)—is expected to decrease synthetase (ECS) and glutathione synthetase (GS), 3.2 Organic Contaminants 61 further suggesting the potential implication of The contaminant’s penetration into the roots glutathione in PCB metabolism. essentially differs from the leaves. Substances pass into roots only through cuticle-free unsuberized cell walls. Roots absorb environmental con- 3.2.2 Hydrocarbons taminants in two phases: • Fast phase: substances diffuse from the sur- Plant uptake of hydrocarbons varies according to rounding medium into the root. hydrophobicity. Hydrophilic compounds (log • Slow phase: gradually distribute and accumu-

Kow < 1) have little afﬁ nity for root membranes, late in the tissues. moderately hydrophobic hydrocarbons (log The intensity of the contaminants absorption

Kow = 1.0–3.0) such as BTEX show high uptake depends on solubility, concentration, molecular efﬁ ciency from soil and groundwater, while mass, polarity and рН. The fate of contaminant

PAHs (log K ow > 4) depict poor uptake as they are depends on its chemical nature, external tempera- strongly sorbed to soil and are therefore not bio- ture, variety of plants and vegetation, etc. available. The degradation of hydrocarbons can Excretion is the simplest way of getting rid of any be via direct or indirect pathway. Direct route organic contaminant entered the plant cell. The involves uptake by a plant, while indirect path- toxicant molecule does not undergo chemical way involves rhizospheric effect where root exu- transformation and, being translocated through dates enhance metabolic degradation and the the apoplast, is excreted from the plant. This release of root-associated enzymes transforms pathway of xenobiotic (contaminant) elimination organic pollutants. The complete degradation of is rather rare and takes place at high concentra- hydrocarbons is brought under aerobic conditions of highly mobile (phloem mobile or ambi- tions. The degradation of petroleum hydrocar- mobile) xenobiotics. Contaminants being bons is mediated by speciﬁ c enzyme system absorbed and penetrated into plant cell undergo (Kvesitadze et al. 2009 ). The oxidative process is enzymatic transformations leading to the increase catalyzed by enzymes oxygenases and peroxi- of their hydrophilicity process simultaneously dases. Monooxygenases and cytochrome P450 accompanied by decreasing of toxicity. Plant enzyme systems play an important role in the cytochrome P450-containing monooxygenases microbial degradation of oil, chlorinated hydro- play an important role in the hydroxylation. carbons, fuel additives and many other com- Cytochrome P450-containing monooxygenases pounds. Plant enzymes such as dehalogenase, use NADPH and/or NADH reductive equivalents nitroreductase, peroxidase, laccase and nitrilase for the activation of molecular oxygen and incor- have been shown to play role in degradation of poration of one of its atoms into lipophilic organic petroleum hydrocarbons. compounds (XH) that results in formation of Plants volatilize contaminants (such as petro- hydroxylated products (XOH). Glutathione leum hydrocarbons) that have been taken up S-transferases are the main group of enzymes through its roots to the atmosphere (phytovolatil- involved in the detoxiﬁ cation of herbicides by ization). It is also applicable to contaminants conjugating them with tripeptide glutathione. such as BTEX, TCE, vinyl chloride and carbon Knuteson et al. (2002 ) suggested dealkylation as tetrachloride (Ndimele 2010 ). the probable mechanism for metabolism of simazine (herbicide) into 2-chloro-4-amino-6- isopropylamino- s -triazine or hydroxysimazine 3.2.3 Herbicides followed by storage of end products in vacuoles.

Stomata play an important role in absorption of toxic compounds. The abaxial side of a leaf, gen- 3.2.4 Explosives erally rich in stomata, absorbs the organic substances particularly herbicides (α-naphthylacetic Studies with Myriophyllum aquaticum demon- acid, 2,4-D, picloram and derivatives of urea). strated aquatic macrophytes possess potential for 62 3 Mechanism of Removal of Contaminants by Aquatic Plants oxidative and reductive metabolism of TNT pH from 3 to 7, sorbed high concentrations of (Pavlostathis et al. 1998 ; Jacobson et al. 2003 ). metals that would usually inhibit bacteria and The rapid sorption/sequestration of explosives remained healthy and viable. such as TNT is followed by: (a) Reduction, resulting in the formation of primary reduction products, namely, Literature Cited 2-amino-4,6-dinitrotoluene (2ADNT) and 4-amino-2,6-dinitroluene (4ADNT) con- Abedin MJ, Feldmann J, Medarg AA (2002) Uptake jugates (Bhadra et al. 1999 ; Best et al. 1999a , kinetics of arsenic species in rice plants. Plant Physiol 128:1120–1128 b ; McCutcheon and Schnoor 2003 ), or Aken BV, Correa PA, Schnoor JL (2010) Phytoremediation (b) Oxidation of TNT facilitated by plausible of polychlorinated biphenyls. New Trends Promis enzymes such as oxygenases, which are the Environ Sci Technol 44(8):2767–2776 cytochrome P450 group of enzymes local- Azqueta A, Shaposhnikov S, Collins AR (2009) DNA oxidation: investigating its key role in environmental ized in microsomes (endoplasmic reticulum) mutagenesis with the comet assay. Mutat Res Genet of plant cells Toxicol Environ Mutagen 674:101–108 Nitroreductase and laccase enzymes break Best EPH, Sprecher SL, Larson SL, Fredrickson HL, down ammunition wastes (2,4,6-trinitrotoluene Bader DF (1999a) Environmental behavior of explosives in groundwater from the Milan army ammuni- or TNT) and incorporate the broken ring struction plant in aquatic and wetland plant treatments. tures into new plant material or organic detritus Uptake and fate of TNT and RDX in plants. that becomes a part of sediment organic matter. Chemosphere 39:2057 The major oxidation products reported so far Best EPH, Sprecher SL, Larson SL, Fredrickson HL, Bader DF (1999b) Environmental behavior of explo- include 2,4-dinitro- 6-hydoxy-benzyl alcohol, sives in groundwater from the Milan army ammuni- 2-amino-4,6-dinitrobenzoic acid and 2,4-dinitro- tion plant in aquatic and wetland plant treatments. 6-hydroxytoluene (Medina et al. 2000 ). The site Removal, mass balances and fate in groundwater of of localization of TNT and metabolites varies TNT and RDX. Chemosphere 38:3383 Bhadra R, Spanggord RJ, Wayment DG, Hughes JB, from submerged to emergent plant species. In Shanks JV (1999) Characterization of oxidation prod- submerged species, leaves are reported as the ucts of TNT metabolism in aquatic phytoremediation major site of compartmentalization, whereas in systems of Myriophyllum aquaticum. Environ Sci emergent species, roots are the major site fol- Technol 33:3354 Brooks RR (1998) Plants that hyperaccumulate heavy lowed by stem and leaves. The rate of removal of metals. CAB International, Wallingford, 384 TNT by plant is rapid and varies with treatment Burken JG, Schnoor JL (1997) Uptake and metabolism of conditions, such as plant density, contaminant atrazine by poplar trees. Environ Sci Technol concentration and temperature. Studies revealed 31:1399–1406 Burken JG, Ma XM, Struckhoff GC, Gilbertson AW that the decline in TNT concentration from the (2005) Volatile organic compound fate in phytoreme- aqueous medium is exponential and follows fi rst- diation applications: natural and engineered systems. order kinetics as assessed by the Michaelis– J Biosci 60:208–215 Menten model, while the uptake of TNT by Calderón-Preciado D, Matamoros V, Bayona JM (2011) Myriophyllum aquati- Occurrence and potential crop uptake of emerging aquatic plants including contaminants and related compounds in an agricul- cum is a mixed, second-order rate that is a func- tural irrigation network. Sci Total Environ 412–413: tion of the mass of the plant (Medina et al. 2000 ). 14–19 Mass balances and pathway analyses have shown Cedergreen N, Madsen TV (2002) Nitrogen uptake by the fl oating macrophyte Lemna minor . New Phytol that nitroreductase and laccase enzymes present 155:285–292 in the root zone break down ammunition wastes Coleman JOD, Blake-Kalff MMA, Davies TGE (1997) specifi cally 2,4,6-trinitrotoluene or TNT and Detoxifi cation of xenobiotics by plants: chemical incorporate the broken ring structures into new modifi cation and vacuolar compartmentation. Trends Plant Sci 2:144–151 plant material or organic detritus that becomes a Coleman JO, Frova C, Schroder P, Tussut M (2002) part of sediment organic matter. During TNT Exploiting plant metabolism for phytoremediation of breakdown, plants such as hornwort increased persistent herbicides. Environ Sci Pollut Res Int 9:18–28 Literature Cited 63

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Land areas which are wet during part or all of the et al. 2008, 2012; Matamoros et al. 2008; year are referred as wetlands. They are of two Pal et al. 2010) and are believed to be natural types: natural and artificial/constructed/man- sinks for many contaminants. Wetlands offer made. Vegetation, soil and hydrology form the important ecological benefits complying with major components of wetlands. Aquatic plant the good chemical status demands by the EU species form a major part of both natural and framework directive. constructed wetlands. Aquatic plant species play an important role in oxygen production, nutrient cycling, water quality improvement and sediment 4.1 Constructed Wetlands stabilization (Mohan and Hosetti 1999). (Man-Made, Artificial or Aquatic plants are preferred over other bio- Engineered Wetlands) logical agents due to their low cost, frequent abundance in aquatic ecosystems and easy han- Constructed wetlands (CW/CTWs) are designed dling. The microbial-rich rhizosphere of wetland to improve water quality and the efficiency is plants is involved in degradation. Wetland tech- dependent on plant processes (Kurzbaum et al. nology gained importance because of its low 2012; Anning et al. 2013). They are formed by the operation and maintenance costs, low greenhouse interaction of biological and physical components effects and energy efficiency. These advantages of the ecosystem capable of removing different make constructed wetlands a cheaper alternative types of contaminants from water. They mimic to conventional treatment methods. Besides sim- the functions of natural wetlands. Constructed plicity of operation and maintenance, treatment wetlands have been used for removing a wide effectiveness, tolerance to fluctuations in hydrau- range of inorganic contaminants, including lic and constituent loading rates, and potential heavy metals, perchlorate, cyanide, nitrate and aesthetic attributes including increased green phosphate, as well as certain organic contami- space, new wildlife habitat and additional recre- nants, including explosives and herbicides, and ational and educational areas also add to this. emerging contaminants such as pharmaceuticals, They have developed a strong potential for appli- fragrances, antiseptics, fire retardants, herbicides cation in developing countries, particularly small and plasticizers (Haber et al. 2003; Birch et al. rural communities. 2004; Braeckevelt et al. 2011; Budd et al. 2011; Wetlands gained attention in recent years due Bustamante et al. 2011; Haarstad et al. 2012). to their inherent capacity for removing pesti- These have been successfully used to treat a wide cides, surfactant, PCPs, pharmaceuticals and variety of wastewaters including petroleum efflu- other microcontaminants (Knight et al. 1993a; ents, pulp and paper wastewater, refinery, and Boreen et al. 2003; Gross et al. 2004; Conkle chlor-alkali effluent, landfill leachates, domestic

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 65 DOI 10.1007/978-81-322-1307-9_4, © Springer India 2013 66 4 Role of Wetlands

Table 4.1 Constructed wetlands implemented successfully at different contaminated sites Site Contaminants Medium References Lake Drainage District of San Se Agricultural subsurface Gao et al. (2003) Joaquin Valley, Corcoran, California, drainage USA Savannah River Site, Aiken, South Fe, Mn Industrial effluent Knox et al. (2006) Carolina, USA Lead–zinc mining facility (Tara Pb, Zn, Fe Mine wastewater O’Sullivan et al. (2004) Mines), Ireland Widows Creek electric utility, Alabama, Co, Ni, Fe, Mn, Cd Coal combustion Ye et al. (1997a, b, c) USA; electrical power station at by-product ash leachate Springdale, Pennsylvania, USA Iowa Army Ammunition Plant, Iowa, TNT Explosives-contaminated Best et al. (1997) USA groundwater Milan Army Ammunition Plant, TNT, RDX Explosives-contaminated Best et al. (1999) and Tennessee, USA groundwater Sikora et al. (1995) San Joaquin Valley, California, USA Se Effluents from oil Hansen et al. (1998) refineries wastewater, municipal wastewater, domestic • Partially treated industrial wastewater sewage, agricultural wastewater, dairy wastewater • Drainage water from mines and mine and drainage (DeBusk et al. 1996a; • Runoff from highways Kadlec and Knight 1996; DeBusk 1998; Kadlec 1998; Sobolewski 1999; Yang et al. 2007; Choudhary et al. 2011; Comino et al. 2011; 4.1.1 Composition of Wetlands Gustavsson, and Engwall 2012; Gunes et al. 2012; Idris et al. 2012; Lin and Han 2012; Sudarsan Vegetation, soil and hydrology are the major et al. 2012; Yu et al. 2012) (Table 4.1). Constructed components of all wetlands. Due to complex wetlands have been found to be effective in treat- interaction in plants, microorganisms, soil matrix ing domestic and municipal wastewater by reduc- and substances in the wastewater, constructed ing suspended solids, organic matter, phosphorus, wetlands have been considered ‘black box’ sys- nitrogen and pathogens (Hencha et al. 2003). tems. Constructed wetlands are of different basic During the last two decades, extensive literature designs featuring different flow characteristics in form of books has been published on various and consist of saturated substrates, vegetation (technical and scientific) aspects of constructed and microbes. Root zone (or rhizosphere) is the wetlands (Jackson 1989; Livingston 1989; Knight active reaction zone of CWs where physicochem- et al. 1993b; Kadlec and Knight 1996; Vymazal ical and biological processes take place by the et al. 1998; Kadlec and Wallace 2008; Matamoros interaction of plants, microorganisms, the soil and Bayona 2008). and pollutants. The rhizosphere of wetland plants Constructed wastewater treatment wetlands provides an enriched culture zone for the can be used to treat wastewater from different microbes involved in degradation. The wetland sources like: sediment zone provides reducing conditions that • Sewage are conducive to the metal removal pathway. The • Municipal wastewater soil is the main supporting material for plant • Septic tanks growth and microbial films. Hydraulic processes • Storm water are influenced by soil matrix. Mixture of sand • Agricultural wastewater (including livestock and gravel produces the best results in terms of waste, runoff and drainage water) both hydraulic conditions and the removal of • Landfill leachate contaminants. Soil physical parameters such as 4.1 Constructed Wetlands (Man-Made, Artificial or Engineered Wetlands) 67 interstitial pore spaces and effective grain sizes tion and wetland shrubs and trees. Free water sur- considerably influence the flow of wastewater in face wetlands vary dramatically in size, from less constructed wetlands—and ultimately the than 1 ha to greater than 1,000 ha. Free water sur- removal of contaminants. face wetlands offer ecological and engineering ben- The removal of contaminants occurs via efit. Free water surface wetlands are used for several mechanisms, including sedimentation, treating agricultural and urban runoff. filtration, sorption, plant uptake and microbial Subsurface flow (SSF) constructed wetlands breakdown. Inorganic and organic constituents (CWs) are one of the most common types of sys- present in wastewaters are treated in wetlands tems used throughout the world. Subsurface flow through various ways: wetlands differ from FWS wetlands in that they • Physically removed through filtration incorporate a rock or gravel matrix so that the • Biologically degraded to non-toxic forms wastewater is passed through in a horizontal or • Absorbed by wetland plants vertical fashion. They consist of beds that are • Adsorbed to media surfaces usually dug into the ground, lined, filled with a • Chemically transformed and stored within the granular medium and planted with emergent mac- wetland matrix rophytes. Wastewater flows through the granular Complex biological and physical environ- medium and comes into contact with biofilms and ments of CWs collectively alter the chemical plant roots and rhizomes. SSF CWs are mainly nature of contaminants. They detoxify wastewa- designed to treat primary settled wastewater, ter by immobilizing and/or transforming pollut- although they are also commonly used to improve ants to less toxic forms. The pollutants may be the quality of secondary effluents. Subsurface taken up into the plant tissues, where they are flow wetlands continue to provide effective treat- accumulated and biotransformed to less toxic or ment of most wastewater constituents through the immobile states and/or volatilized to the atmo- winter in temperate climates. Contaminants are sphere (Hansen et al. 1998; Qian et al. 1999; Zhu removed from wastewater in SSF CWs by physi- et al. 1999). In CWs treating domestic wastewa- cal, chemical and biological processes (García ters, emerging contaminants are reported to be et al. 2010). Redox conditions prevailing in SSF eliminated by photodegradation, biodegradation, CWs are linked to contaminant removal mecha- sedimentation, plant uptake and/or adsorption nisms. The main biological processes linked to (Matamoros and Bayona 2008). Apart from this, organic matter transformation—aerobic respira- natural, restored and created wetlands that are fed tion, denitrification, acid fermentation, sulphate with natural waters are also impacted by urban reduction and methanogenesis. They are mainly and agricultural runoff. Metalloids like Se and As involved in removal of surfactants, pesticides and can be transformed by both biological and chem- herbicides, emergent contaminants, nutrients and ical processes to a variety of forms that differ in heavy metals. Subsurface flow wetlands are the mobility and toxicity (Terry et al. 2000). common system design implemented in Europe for domestic wastewater treatment, while in the United States (North America), the FWS type is 4.1.2 Types of Wetlands more common (DeBusk and DeBusk 2001). FWS wetlands can commonly occur in communities Treatment wetlands are generally classified as either with 1,000 or fewer people to a population greater free water surface (FWS) or subsurface flow (SSF) than 1 million in cities. systems. Free water surface wetland (FWS) encom- Subsurface flow constructed wetlands are passes shallow water flowing over plant media further subdivided into two types: mainly mineral (sandy) or organic (peat) soils (a) Horizontal surface flow systems (HSF)— underneath vegetation. Vegetation mainly consists Wastewater is maintained at a constant depth of marsh plants, such as Typha and Scirpus, but may and flows horizontally below the surface of also include floating and submerged aquatic vegeta- the granular medium (Vymazal 2006). 68 4 Role of Wetlands

Wetlands the large-scale treatment wetlands in south Florida, collectively known as the Stormwater Treatment Areas, have been constructed to reduce Horizontal Vertical P levels in agricultural runoff. A front-end treat- Functioning does not affect Functioning improves the ment cell (dominated by T. domingensis and/or aeration of the bed aeration of the bed T. latifolia with other EAV and FFAV species) is Require less oxidized conditions Operate under more oxidized used initially to treat runoff, and a back-end treat- for operation conditions ment cell (dominated by C. demersum, N. guada- Limited nitrification capabilities Produce nitrified effluents lupensis, Chara sp. and/or Hydrilla verticillata) Less efficient More efficient is expected to reduce further P concentration of Treat limited number of Treat higher number of contaminants contaminants the effluent from the front-end cell. Some treatment wetlands have been con- Fig. 4.1 Difference between horizontal and vertical structed that combine different wetland types. wetlands These include 134-ha Eastern Service Area wetland in Orlando, FL, which consists of con- (b) Vertical flow systems (VFS)—Wastewater is structed FWS wetlands that are followed by distributed over the surface of the wetland natural forested wetlands. Hybrid systems are and trickles downwards through the granular based on need of specific contaminant removal. medium (Fig. 4.1). Enhanced nitrogen removal in SSF wetlands cre- Vertical systems can further be sorted in four ate an oxygenated environment that enhances types depending on the hydraulic regimes: unsat- nitrification in the rock or gravel matrix. Many urated flow, permanently saturated flow, intermit- subsurface wetlands accomplish this by sequenc- tent unsaturated flow and flood and drain ing horizontal flow beds with vertical flow beds wetlands. Concerns over matrix clogging and the to enhance nitrification (DeBusk and DeBusk potential high cost of renovation also limit the 2001). Vertical flow beds have been combined deployment of extremely large SSF wetlands. to get enhanced removal of COD and nitrogen (Fig. 4.2). 4.1.2.1 Hybrid Treatment Wetlands Two or more different types of wetlands are often combined to form hybrid wetlands to get higher 4.1.3 Major Wetland Species removal efficiency. It is comprised of VF and HF beds that are arranged in a two-stage pattern to Macrophytes play an important role in wetlands. achieve higher treatment efficiency and is most Emergent, submerged and/or free-floating aquatic widely used in Europe (Vymazal 2005; Kadlec species form a part of both natural and and Wallace 2009). FWS wetlands have recently constructed wetlands (Brix 1994, 1997). The been hybridized with other VF and/or HF wet- common species include Scirpus maritimus, lands to improve nutrient and bacteria removal Scirpus cyperinus, Scirpus robustus (salt marsh efficiency, to reduce the acreage necessary for bulrushes), Polypogon monspeliensis (rabbitfoot target pollutant removal and/or to enhance habi- grass), Typha angustifolia, Typha latifolia (cat- tat quality and ancillary benefits such as wildlife tail), Typha orientalis, Typha minima, Juncus conservation and recreation (Vymazal 2005; xiphioides (Irish-leaved rush), Phragmites Fleming-Singer and Horne 2006; Rousseau australis (Cav.) Trin., Myriophyllum spicatum, et al. 2008). A hybrid wetland also incorporates Elodea sp., Pontederia cordata L., Cyperus FWS wetlands dominated by free-floating aquatic alternifolius, Acorus calamus, Iris pseudacorus, vegetation (FFAV), emergent aquatic vegetation Lythrum salicaria, Arundo donax, Juncus (EAV) or submerged aquatic vegetation (SAV) effusus, Azolla sp., Lemna sp. and Eichhornia communities to achieve higher treatment effi- crassipes. Submerged aquatic vegetation spe- ciency, particularly for P removal. For example, cies, such as Ceratophyllum demersum, Elodea 4.1 Constructed Wetlands (Man-Made, Artificial or Engineered Wetlands) 69

Types of wastewater

Municipal/domestic Countries

Agricultural – Swine USA Free Dairy Canada water Stormwater runoff - Australia surface Highway UK Airport Sweden Agricultural Spain Urban Kenya Types of Dairy Greece Vertical Constructed Mine drainage- Norway flow (VF) Wetlands Acid coal mine China Copper mine India Gold mine Italy Uranium mine France Germany Industrial- Refinery Portugal Horizontal Paper and pulp South Africa flow (HF) Textiles New Zealand Sugar Explosives Tannery Food processing Petrochemical Distillery Landfilll leachate

Fig. 4.2 Types of wetlands for removing wastewaters from different sources nuttallii, Potamogeton pusillus and Najas of transformation and fixation of metals. In guadalupensis are present in many natural and subsurface flow systems, aerobic processes only constructed wetlands (Chen 2011). predominate near roots and on the rhizoplane Free water surface wetlands comprise of (the surface of the roots). In the zones that are macroscopic vegetation such as Typha and largely free of oxygen, anaerobic processes such Phragmites, but more often they contain a diver- as denitrification, sulphate reduction and/or sity of other emergent and floating plants such as methanogenesis take place. Pontederia, Sagittaria, Eleocharis, Utricularia and Lemna. Subsurface flow wetlands usually remain dominated by the species Phragmites, 4.1.4 Factors Affecting Functioning Scirpus and Typha. It is difficult to establish of Wetlands seeds and other propagules on the bed’s surface because of high organic loading provided to SSF 1. The supply of oxygen plays a crucial role in systems. Typha latifolia have been used success- the activity and type of metabolism performed fully to treat groundwater contaminated with by microorganisms in the root zone. explosives and heavy metals from coal combus- 2. Selection of plant species to use in CWs is tion by-product leachate. The growth and adapta- important, since plants are involved in the tion of plants to the anoxic conditions in wetland input of oxygen into the root zone, uptake of sediments drives many of the degradation pro- nutrients and direct degradation of pollutants. cesses (Horne 2000). For example, the activity of 3. The input of carbon from plants into their the plant roots alters the chemical conditions rhizosphere is known as rhizodeposition. of the surrounding sediment, enhancing the rate Rhizodeposition products (exudates, mucigels, 70 4 Role of Wetlands

dead cell material, etc.) cause various biological phytodegradation, rhizodegradation and processes to take place in the rhizosphere. phytovolatilization processes. Wetland plants The chemical composition of the exudates is readily take up essential nutrients, such as very diverse. Root exudates are sugars and nitrate, ammonium and phosphate and metals vitamins such as thiamine, riboflavin and (Cheng et al. 2009a, b). The rate of contami- pyridoxine; organic acids such as malate, nant removal by plants varies widely, depend- citrate, amino acids, benzoic acids and phe- ing on the plant growth rate and the nol; and other organic compounds. The range concentration of the contaminant in the plant of substances varies from one species to other. tissue. Woody plants, trees and shrubs provide Sugars and amino acids can be used by micro- relatively long-term storage of contam organisms as substrates, and excreted vitamins inants compared with herbaceous plants. stimulate microbial growth. Furthermore, it Contaminant uptake rate per unit area of land has been shown that organic compounds is often much higher for herbaceous macro- released by plants and plant residues influence phytes such as Typha. Algae also provide a the microbial degradation of xenobiotics significant amount of nutrient uptake but are (Horswell et al. 1997; Moormann et al. 2002). relatively susceptible to the toxic effects of heavy metals. Bacteria and other microorganisms also provide uptake and short-term stor- 4.2 Mechanism of Contaminant age of nutrients and some other contaminants Removal by Wetlands in the soil (Stottmeister et al. 2003). Plants directly take up contaminants into their root Wetlands encompass many processes and mecha- structure and secrete substances that add to nisms in the removal of contaminants. The basic biological degradation, and contaminants that three are physical, biological and chemical entered the plant biomass are transpired removal processes. through the plant leaves. Microorganisms in 1. Physical processes—They are often used in wetland soils take up and store nutrients but primary treatment of wastewater. Surface the metabolic functions assist in organic pol- water typically moves very slowly through lutant removal. The bacteria, mostly present wetlands due to the characteristic broad sheet in soil, use the carbon found in organic matter flow and the resistance provided by rooted and as an energy source and convert to carbon floating plants. Water that flows through wet- dioxide in aerobic conditions and methane in lands moves rather slowly due to resistance anaerobic conditions. The microbial metabo- from plant matter and a uniform sheet flow of lism is also very important in the removal of water. The plants in the wetland help trap sed- inorganic nitrogen (DeBusk 1999a). iment (DeBusk 1999a). By using gravity and 3. Chemical processes—This process includes the differences in relative densities of sus- sorption, photo-oxidation, and volatilization. pended material, particles are allowed to settle Sorption is the most important chemical pro- in the wetland. Mats of floating plants in wet- cess which results in short-term retention or lands may serve as sediment traps, but their long-term immobilization of several classes of primary role in suspended solids removal is to contaminants. It involves the moving of limit resuspension of settled particulate mat- charges or transfer of ions (or molecules with ter. Sedimentation of suspended solids is pro- positive or negative charges) from the aqueous moted by the low flow velocity and by the fact phase (water) to the solid phase (soil). that the flow is often laminar (not turbulent) in Sorption includes the processes adsorption wetlands. and precipitation. Adsorption refers to the 2. Biological processes—It represents a promi- attachment of ions to soil particles, either by nent pathway of contaminant removal in cation exchange or chemisorption. Cation wetlands (DeBusk 1999a). This involves exchange involves the physical attachment of 4.3 Contaminants Removed by Wetlands 71

cations, or positively charged ions, to the sur- immobilizing and/or transforming pollutants to faces of clay and organic matter particles in less toxic forms (Fig. 4.3). the soil. Cations are bonded to the soil by electrostatic attraction. Many contaminants in wastewater and runoff exist as cations. Cation 4.3.1 Inorganic Contaminants exchange capacity (CEC), i.e. capacity of soils for retention of cations, generally Wetlands have shown capacity to treat inorganic increases with increasing clay and organic contaminants such as metals, nutrients and matter content. Photo-oxidation utilizes the radionuclides. power of sunlight to break down and oxidize compounds. Volatilization breaks down the 4.3.1.1 Metals compound and expels it into the air as a gas- Metal (Al, As, Cd, Co, Cu, CN-, Fe, Pb, Mn, Ni, eous state (DeBusk 1999a; DeBusk and U and Zn) removal in natural wetlands has been DeBusk 2001). widely reported (Hadad et al. 2010; Knox et al. 2010; Marchand et al. 2010; Lesage et al. 2007a, b; Groza et al. 2010; Dotro et al. 2012). Metal 4.3 Contaminants Removed removal in wetlands depends on the type of ele- by Wetlands ment, their ionic forms, substrate conditions, season and plant species. Metal removal in In CWs, domestic wastewaters and emerging wetlands occurs by plant uptake, soil adsorption, contaminants are eliminated by photodegra- precipitation and cation exchange through plant- dation, biodegradation, sedimentation, plant induced chemical changes in rhizosphere. uptake and/or adsorption (Matamoros and The major mechanisms of metal removal in Bayona 2008). Wastewater is detoxified by wetlands have been summarized as follows:

Municipal Hexachlorobenzene, COD, BOD, TSS, K, Ca Phragmites australis, Typha latifolia

Tannery Cr, Ni, TSS, BOD,COD Phragmites australis

Dairy COD, BOD, TSS, estrogens, androgens, N, Arundo donax, Phragmites australis

Piggery COD, BOD, TSS, TN, TP Phragmites australis

Wastewaters Textile Cr and other metals Phragmites australis

Storm Nitrate, metals Typha latifolia, Sagittaria latifolia

Eutrophic TN, TP Canna chineresis, Typha latifolia

Domestic Chlorpyrifos, DOC, TSS, TP, TN, BOD Phragmites australis

Saline hexachlorobenzene, COD, BOD, TSS, K, Ca Typha latifolia

Fig. 4.3 Types of wastewaters treated by wetlands. (COD Chemical oxygen demand, BOD Biochemical oxygen demand, TN total nitrogen, TP total phosphorus, TSS total suspended solids, DOC Dissolved organic carbon) 72 4 Role of Wetlands

• Sorption and/or exchange onto organic matter iron hydroxides or by coprecipitating with iron (detritus) oxyhydroxides. Absorption and deposition of • Filtration of solids and colloids suspended solids in sediments is followed by • Formation of carbonates accumulation of some amount by plants and bac- • Association with iron and manganese oxides teria (Kadlec and Knight 1996). The efficiency of • Metal hydrolysis (catalyzed by bacteria under systems depends strongly on (1) inlet metal acidic conditions) concentrations and (2) hydraulic loading (Kadlec • Reduction to nonmobile forms (also catalyzed and Knight 1996). by bacteria) Metals can also form insoluble compounds • Formation of insoluble metal sulphide precip- through reduction. Under chemically reducing itates resulting from microbial reduction conditions (Eh < 50 mV), sulphates can be • Biological methylation followed by reduced to sulphides. Reductive conditions into volatilization the substrate (Dorman et al. 2009) promote mas- • Ion-exchange capacity of the mineral and sive ion release, particularly of Fe and Mn, into humic fractions of soil the water by reduction of the oxides and oxyhy- • Accumulation into plant matter droxides trapped in the substrate. Precipitation of • Coprecipitation of some elements such as metal as oxides or adsorption onto organic matter arsenic with iron is dependent upon redox potential. At redox Lesage et al. (2007b) reported adsorption and potential above 100 mV, metal oxides are precipitation as insoluble salts (mainly sulphides reduced, resulting in a release of dissolved met- and oxyhydroxides), deposition and rhizosphere als, while below 100 mV, metals may be mainly activity as the main mechanisms for metal associated with sulphides. Most macrophytes removal. Adsorption is an important mechanism play a role in maintaining oxidizing conditions for removal of metals in wetlands. It involves by shoot-to-root oxygen transport. Such condi- transfer of ions from a soluble phase to a solid tions promote formation of iron oxides, hydrox- phase and results in short-term retention or long- ides and oxyhydroxides, such as the iron plaques, term stabilization. Metals are adsorbed to parti- and consequently result in metal removal by cles of fine-textured sediments and organic matter adsorption and coprecipitation. Since As(III) is by either ion exchange depending upon factors more mobile and toxic than As(V), active As such as the type of element or the presence of remediation may require conversion of As(III) to other elements competing for adsorption sites As(V) in the rhizosphere and subsequent immo- (Seo et al. 2008). Metals such as Fe, Al and Mn bilization of As(V) by adsorption or coprecipita- form insoluble compounds through hydrolysis tion (Guan et al. 2009). Fe oxides in the and/or oxidation. This leads to formation of a rhizosphere have a strong adsorptive capacity for range of oxides, oxyhydroxides and hydroxides arsenate. Arsenic is not the only inorganic ion (Sheoran and Sheoran 2006). Fe(II) can be oxi- present in natural waters, and adsorption of dized to Fe(III) which can deposit onto root sur- As(V) and As(III) oxyanions by ferric hydroxide faces of aquatic macrophytes (Weiss et al. 2003), may be adversely affected by anions such as forming plaques with a large capacity to adsorb carbonate, sulphate, phosphate and silicate and metals (Cambrolle et al. 2008), aided by the also by organic matter. action of Fe(II)-oxidizing bacteria. Fe(III) can Metals may also form metal carbonates. precipitate to produce oxides, hydroxides and Although carbonates are less stable than sul- oxyhydroxides. Fe(II) can also precipitate as phides, they can contribute to initial trapping of oxides (Jonsson et al. 2006) or coprecipitate with metals (Sheoran and Sheoran 2006). The pH other metals such as Zn, Cd, Cu or Ni (Matagi strongly affects the efficiency of metal removal in et al. 1998). Arsenic may also be removed from wetlands. Ammonium conversion into nitrites the water column by adsorbing onto amorphous during nitrification leads to proton production. 4.3 Contaminants Removed by Wetlands 73

These hydrogen ions are then neutralized by of metal sulphides in an organic substrate bicarbonate ions. Macrophytes, in releasing improves water quality by decreasing the mineral oxygen, promote the nitrification process. Protons acidity without causing an increase in proton produced due to nitrification may not all be acidity (Sheoran and Sheoran 2006). Macrophytes - neutralized by HCO3 ions, resulting in a pH transport oxygen to their rhizosphere. This, cou- decrease. Alkaline conditions are necessary to pled with the action of nitrifying bacteria such as promote coprecipitation of cationic metals, such Nitrosomonas spp. and Nitrobacter spp., enables as Cu, Zn, Ni and Cd. A high rate of nitrification ammoniacal N removal of the soil environment can therefore reduce the efficiency of a constructed (Lee and Scholz 2007). Furthermore, oxidizing wetland in terms of cationic metal removal. In soil conditions promote formation of iron oxides, the special case of acid mine drainage, the water hydroxides and oxyhydroxides and consequently and substrates are characterized by high metal result in metal removal by coprecipitation. concentrations and a low pH. Metal removal have been reported by Macrophytes, such as Phragmites australis, Phragmites australis, Phragmites karka, Phalaris promote sedimentation of suspended solids and arundinacea, Typha domingensis and Typha lati- prevent erosion by decreasing water flow rates folia (Lesage et al. 2007a; Vymazal et al. 2007; by increasing the length per surface area of the Maine et al. 2009; Scholz and Hedmark 2010). hydraulic pathways through the system (Lee and Metals are efficiently removed by plants, and this Scholz 2007). Under static conditions, the wetland mainly occurs by immobilizing them in the rhi- behaves like a stagnant pond in which displace- zosphere and storage in the below-ground bio- ment effects caused by submerged plant mass mass (Baldantoni et al. 2009; Zhang et al. 2010). decrease retention times. Retention times increase Macrophytes remove only a small amount of with increasing vegetation density, thus enabling metals most of which is taken up by root and only better sedimentation. Flocs may adsorb other types a small amount is transported to shoot (Lee and of suspended materials, including metals. Scholz 2007). Poor translocation may be due to Rhizosphere bacteria possess an ability to uti- sequestration of most of the metals in the vacu- lize efficiently growth substrates available in the oles of root cells to escape toxic effects. Plants rhizosphere and to cope with toxic environments trap metals into the substrate via rhizodeposition due to the presence of detoxifying enzymes (Kidd et al. 2009). Root-exuded organic acids (Chaudhry et al. 2005). The genera commonly such as citrate, oxalate, malate, malonate, fuma- found in rhizospheres include Rhizobium, rate and acetate chelate metallic ions to varying Azotobacter and Pseudomonas. Besides forming degrees and thus decrease their phytotoxicity a habitat for microorganisms, plant roots also (Chaudhry et al. 2005). Floating aquatic plants provide substrates such as sugars in exchange for provide good metal absorption (Vymazal et al. phosphate or nitrogen (N2 fixation). Organic 1998). The species include Eichhornia crassipes, compounds exuded by the roots, fungi and bacte- Pistia stratiotes and Salvinia herzogii (Maine ria, e.g. saponins, proteins and enzymes, may et al. 2001, 2004; Suné et al. 2007; Dhote and mobilize soil-born pollutants, including metals. Dixit 2009). Floating plants do not actively pro- Sulphate-reducing bacteria such as Desulfovibrio mote metal adsorption to the substrate, but store spp. take part in the reduction of sulphates to sul- them into their biomass. Submerged aquatic phites and subsequently to sulphides (Garcia plants such as Potamogeton spp., Ceratophyllum et al. 2001). Then these sulphides react with met- demersum, Myriophyllum spicatum and Hydrilla als such as Cu, Zn and Fe to form insoluble pre- verticillata possess high potential to decontami- cipitates (Murray-Gulde et al. 2005b). Optimal nate water (Bunluesin et al. 2007). Nyquist and conditions for sulphate-reducing bacteria are Greger (2009) proposed to use submerged plants redox potentials lower than 100 mV and pH to stabilize acid mine drainage because these greater than 5.5 (Garcia et al. 2001). Precipitation plants take up more metals, using their whole 74 4 Role of Wetlands biomass. Submerged macrophytes are probably mentation of constructed wetlands for removing not suitable for the conditions prevailing in acid significant levels of trace elements such as mine drainage because of excessive Fe precipita- selenium (Se) from the effluents was seen at oil tion onto their surfaces, which inhibits light pen- refineries at San Francisco Bay Delta and Tulare etration and photosynthesis (Nyquist and Greger Lake Drainage District of San Joaquin Valley, 2009). Removal of metals (Al, As, Cd, Co, Cu, California. Some proportion of the soluble Se Fe, Pb, Mn, Ni, Se, U and Zn) present in mine entering the wetland became chemically reduced drainage have been documented. Aquatic macro- and bound to sediments, but a major portion of it phytes play an essential role in creating the envi- was absorbed by plants, accumulated in roots and ronment for metal uptake, but their removal of volatilized. The plants and microbes (present in metals usually accounts for a minor proportion of the roots) took up Se mainly in the form of sele- the total mass removed. Metals such as Al, Fe nate or selenite and metabolized it to volatile and Mn are often removed by hydrolysis. The forms like dimethyl selenide (DMSe), which resulting acidification of water buffered by alka- escaped to the atmosphere, minimizing the linity produced in wetland sediments by anaero- effects to other components of food chain. The bic bacteria. Bacterial sulphate reduction process was referred as biological volatilization. accounts for much of this alkalinity. It can also Volatilization of Se involves the assimilation of contribute significantly to metal removal by for- inorganic Se into the organic selenoamino acids mation of insoluble sulphides. Other important selenocysteine (SeCys) and selenomethionine processes include the formation of insoluble car- (SeMet) (Hafeznezami et al. 2012). Accumulation bonates, reduction to nonmobile forms and in plant tissues accounted for only 2–4 %, while adsorption onto iron oxides and hydroxides. 3 % of the Se was removed by biological volatil- Wetland plants can accumulate heavy metals ization to the atmosphere. Cattail, Thalia and rab- in their tissues. Previous studies indicated that bitfoot grass are highly tolerant species and some wetland plants have the ability to take exhibit no growth retardation. In the aqueous up > 0.5 % dry weight (DW) of a given element phase of surface flow wetlands to treat mine and bioconcentrate the element in its tissues to drainage, Fe(II) is oxidized to Fe(III) by abiotic 1,000-fold the initial element supply concentra- and microbial oxidation. Other heavy metals are tion. For instance, duckweed (Lemna minor) and immobilized in the mainly anoxic soil by micro- water hyacinth (Eichhornia crassipes) are excel- bial dissimilatory sulphate reduction and the H2S lent accumulators of Cd (6,000–130,000 mg kg−1 formed. Constructed wetlands using emergent DW) and Cu (6,000–7,000 mg kg−1 DW) (Zayed plant species such as Scirpus cyperinus, et al. 1998; Zhu et al. 1999). The plants are Myriophyllum spicatum and Typha latifolia have capable of storing large amounts of metals in been used successfully to treat groundwater con- plant biomass and in its roots (DeBusk 1999b). taminated with heavy metals from coal combus- Many wetland plants accumulated higher con- tion by-product leachate. centrations of metals in roots than in shoots Carex pendula, a common wetland plant (Ye et al. 1997a, b, c; Deng et al. 2004, 2006). found in Europe, accumulated considerable Hyperaccumulators have been part of many wet- amounts of Pb, particularly in root biomass, and lands. Constructed wetlands have been used for contributed to cleanup of Pb contaminated removing significant levels of trace elements wastewaters. The wetland system efficiently such as Se, As and B from the effluent (Terry removed U (95 %) from contaminated water et al. 2000; Ye et al. 2003). Plants are used in from the tailing pond located near U processing conjunction with microbial activity associated plant. Typha domingensis used in constructed with the plants to extract, accumulate and volatil- wetland receiving metallurgical effluent showed ize Se. Once absorbed by plant roots, Se is trans- higher affinity for metal (Cr, Ni and Zn) and total located to the shoot where it may be harvested phosphorus removal. The chlorophyll concentra- and removed from the site. A successful imple- tion showed maximum sensitivity to effluent 4.3 Contaminants Removed by Wetlands 75 toxicity in comparison to other parameters such cess of uptake/removal. For example, the uptake as biomass and plant height. The highest root and of Cr6+ by Eichhornia crassipes subsequently stele cross-sectional areas, number of vessels and results in the reduction of toxic Cr6+ to less toxic biomass registered in inlet plants promoted the Cr3+. The root surface of wetland plants possesses uptake, transport and accumulation of contami- some specialized structures called metal-rich rhi- nants in tissues. The adaptability of T. domingen- zoconcretions or plaques, which are mainly com- sis to the prevailing conditions in the constructed posed of iron hydroxides and/or Mn, which are wetland allowed it to become the dominant spe- immobilized and precipitated on the root surface. cies and enabled the wetland to maintain a high The plaques restrict metal uptake at low pH con- contaminant retention capacity. The pattern of ditions but enhance that at higher pH (Dhir et al. metal distribution in wetland plants is suitable to 2009; Dhir 2010). The rhizosphere associated restrict metals being transported from roots to with the plants also plays an important role in the shoots. However, the degree of upward transloca- degradation and breakdown of contaminants. tion is dependent on plant species, particular Plants resist excessive exposure through sev- metal and a number of environmental conditions, eral routes. One mechanism is biomineralization such as pH, redox potential (Eh), temperature onto roots leading to metal precipitation. Another and salinity (Fitzgerald et al. 2003; Fritioff is formation of complexes with glutathione et al. 2005). In addition, other factors, such as (GSH) and transport into the vacuole (e.g. soil particle size, organic matter content, nutri- unidentified ATP-binding cassette transporter of ents and the presence of other ions may also As(III)-GS3 or Cd(II)-GS2 (Verbruggen et al. influence metal uptake by wetland plants 2009)) where high molecular weight complexes (Greger 1999). The soils present in the wetland (HMWC) may be formed that contain sulphides immobilize heavy metals in a highly reduced (S2_). The third is production of organic ligands sulphite or metallic form. The roots act as filters, rich in cysteine and non-protein thiols (NP-SH), removing suspended particles from the water such as phytochelatins (PC) and metallothioneins through mechanical and biological activity. (MT). Phytochelatins chelate metals and com- Phytostabilization is the major approach for plexes to be transported into the vacuoles (Pal immobilization of metals in plants and storage in and Rai 2010). Metallothioneins and metallo- below-ground parts such as root and soil, while chaperones contribute to maintain the homeosta- phytoextraction involves the use of hyperaccu- sis, bind metals and protect against oxidative mulators to remove metals. Ion uptake results stress. The fourth mechanism is hyperactivity of from the contact of the plant with the medium antioxidant systems to minimize reactive oxygen and occurs directly through leaf cells. The site of species (ROS) (Sharma and Dietz 2009). metal accumulation and form in which they are Potamogeton pusillus responds positively to short absorbed varies from species to species. The sub- Cu exposure by inducing activity of antioxidant merged aquatic plant species such as Elatine tri- enzymes like glutathione peroxidase (GPX), glu- andra accumulate heavy metals such as As tathione reductase (GR) and peroxidase (POD) mainly in organic forms (e.g. methylarsonic acid (Monferran et al. 2009). In Najas indica exposed and methylarsinic acid), while semiaquatic plant to Pb, the activities of antioxidant enzymes such species such as Spartina alterniflora and Spartina as superoxide dismutase (SOD), ascorbate patens accumulate inorganic arsenic in roots, and peroxidase (APX), guaiacol peroxidase (GPX), organic form dimethylarsenic acid is translocated catalase (CAT) and glutathione reductase (GR) to shoots. were elevated along with the induction of the The tolerance mechanism in plants includes antioxidants GSH, cysteine, ascorbic acid and the sequestration of metals in tissues or cellular proline (Singh et al. 2010). Iris pseudacorus also compartments (vacuoles), restricting the move- responds to Pb and Cd exposure by enhancing ment to shoots (avoidance). The plant species POD activities and proline concentrations in also tend to alter speciation of metals in the pro- roots and shoots. Exposure of Egeria densa to Cd 76 4 Role of Wetlands resulted in both a formation of thiol-enriched Cd authors concluded that Typha relies more on complexing peptides and a synthesis of low thiol induction and metal binding for metal molecular weight, unidentified metal chelators in avoidance, while Phragmites is based on shoots. Cd and Cu exposure also lead to coordi- increased antioxidant enzyme activities and nated responses of PC synthase (PCS) and MT thus scavenging of active oxygen species. genes in black mangrove Avicennia germinans. (d) Presence of microbial symbionts in rhizo- Both MT and PCS gene expression increased in sphere soils. The presence of periphyton A. germinans leaves in response to metal expo- associated with the root of P. australis in sure, which supports the hypothesis that MTs and freshwater wetlands enhanced the ability of PCS are part of the metal tolerance mechanism in the reed to accumulate and retain metals. this species (Gonzalez-Mendoza et al. 2007). However, Khan et al. (2000) suggested that Wetland plants tolerate heavy metals by vari- mycorrhizae play a protective role, restrict- ous means such as (Yang and Ye 2009) the ing the uptake of metals by plants through following: immobilizing metals in the fungal tissues. (a) Restricting upward movement into shoots (e) Iron plaque as a barrier to heavy metals. Fe and translocation of excessive metals into old plaque may act as a barrier to toxic metals. leaves before shedding or secreting excessive Otte et al. (1989) found that a heavy coating metals by special organs such as salt glands. of Fe plaque may act as a barrier to Zn Some studies show that Avicennia marina uptake. Iron plaques have also been shown to and Spartina alterniflora can excrete metals act as a filter for the movement of Fe, Cu, Zn, in salt crystals released through hydathodes Ni and Cd into rhizomes and shoots. This (salt glands) (Kraus 1988; MacFarlane and may be achieved by adsorption onto Fe com- Burchett 2000). pounds or coprecipitation (Bostick et al. (b) Sequestering heavy metals in organs or sub- 2001; Hansel et al. 2002). However, other cellular compartments with little or no sensi- studies have shown that Fe plaque does not tive metabolic activity. Vesk et al. (1999) impede the uptake of toxic metals although it found that Cu and Zn mainly localized inside can immobilize metals. cells of roots of free-floating water hyacinth Usefulness in large-scale constructed wet- (E. crassipes), with a less but significant lands is uncertain, particularly due to their amount in the stele cell wall, whereas Zn and low winter performance and the necessity for Cu increased centripetally in the stele cell harvesting biomass in order to maintain an walls. In the roots of grey mangrove efficient system (Kivaisi 2001). On the other (Avicennia marina), metals (Cu, Pb and Zn) hand, the role of plants as suppliers of organic were concentrated predominantly in cell matter is far more important, and so differ- walls (MacFarlane and Burchett 2000). ences in metal accumulation between the two (c) Synthesizing phytochelatins (PCs), peptides types are minor. and exudates to chelate-free metal ions or Microorganism-mediated alteration of metals increasing antioxidant enzyme activities. occurs via oxidation and reduction. Furthermore, Fediuc and Erdei (2002) studied the phy- oxidizing soil conditions promote formation of siological and biochemical aspects of iron oxides, hydroxides and oxyhydroxides and Cd-protective mechanisms induced in P. aus- consequently result in metal removal by tralis and T. latifolia. Different defence strat- coprecipitation. Bacteria participate in oxidation egies were operated by the two species under of sulphides to sulphites and then to sulphates. Cd stress. In Typha, the increasing accumula- Because sulphides take part in metal coprecipitation of Cd was in positive correlation with tion in the substrate, oxidation may lead to metal the increases in free thiol content, while in mobilization. Under reducing conditions, Phragmites, glutathione reductase, catalase sulphate-reducing bacteria such as Desulfovibrio and peroxidase activities were increased. The spp. take part in the reduction of sulphates to 4.3 Contaminants Removed by Wetlands 77 sulphites and subsequently to sulphides. Then tribute to metal trapping into the substrate via these sulphides react with metals such as Cu, Zn rhizodeposition. and Fe to form insoluble precipitates. Optimal conditions for sulphate-reducing bacteria are 4.3.1.2 Nitrogen redox potentials lower than 100 mV and pH Nitrate removal in wetlands is usually very high greater than 5.5. Precipitation of metal sulphides (DeBusk 1999b; Correa-Galeote et al. 2013; Lee in an organic substrate improves water quality by et al. 2012). The removal of nitrogen using decreasing the mineral acidity without causing an wetlands involves a number of processes. These increase in proton acidity. processes include ammonia volatilization, ammonification, nitrification, denitrification, plant and Role of Plants microbial uptake, ammonia adsorption, organic Macrophytes are key players in wetlands, both nitrogen buria l and ANAMMOX (anaerobic natural and constructed. Plant-derived organic ammonia oxidation). All processes reduce the matter in wetlands over time continuously pro- amount of nitrogen in the system. Nitrogen vides sites for metal sorption, as well as carbon removal in wetlands occurs from direct assimila- sources for bacterial metabolism, thus promoting tion by plants and through microbial nitrification long-term functioning. and denitrification. The spatial distribution of the N-cycling microbial communities of sediments Emergent Plants was heterogeneous and complex. Nitrogen exists Several emergent plants have been tested in con- in many forms such as inorganic and organic structed wetlands, achieving variable metal forms. Inorganic nitrogen includes nitrates, removal rates. Phragmites australis is the spe- nitrites and ammonium. In natural environments cies used most. Phalaris arundinacea displays where oxygen is in surplus, nitrogen usually capacities similar to Phragmites australis, as do exists as nitrates and nitrites. In environments Typha domingensis, Typha latifolia and that lack oxygen, nitrogen is available as ammo- Phragmites karka. Suspended organic matter nium in wetland soils. Nitrogen present in wet- and metals are efficiently removed in the pres- lands is either taken up by plants or broken down ence of plants mainly by immobilization in the by microorganisms. Plants use nitrates and rhizosphere and storage in the below-ground ammonium as nutrients which can be stored as biomass (Baldantoni et al. 2009; Zhang et al. organic nitrogen. Microorganisms break down 2010; Abou-Elela and Hellal 2012). The highest inorganic nitrogen mostly by denitrification plant metal concentrations occur in the winter in which convert nitrate to nitrogen gas. Ammonia rhizomes (Baldantoni et al. 2009), but overall, taken up by plants is converted to nitrate by less than 2 % of the trapped metals are stored in nitrification. the plant biomass (Lee and Scholz 2007). Steps involved in nitrogen removal in wet- Therefore, macrophytes are not important sinks lands include the following: for metal removal. Generally, only a small 1. Ammonification—It is the process where amount of metals taken up by roots is trans- organic nitrogen is converted to ammonia. ported to the shoots. Long-distance transloca- The process converts amino acids into ammo- tion of metal ions between roots and shoots is nia. The majority of ammonification is done summarized elsewhere (Lu et al. 2009). Poor by anaerobic and obligate anaerobic mineral- translocation may be due to sequestration of ization. The rates of ammonification depend most of the metals in the vacuoles of root cells, on temperature, pH, C/N ratio, available nutri- which may be a natural response to alleviate ents and soil conditions. This step is crucial potentially toxic effects (Shanker et al. 2005). before ammonium is then absorbed by plants, However, other studies have shown that metals solubilized and returned to the water column, such as Cr are efficiently stored into the whole converted to gaseous ammonia or aerobically plant (Zhang et al. 2010). Plants certainly con- nitrified by aerobic organisms (EPA 1999). 78 4 Role of Wetlands

2. Nitrification—Ammonia is biologically oxi- Nitrification is effected by factors like avail- dized to nitrite and then finally to nitrate. ability of dissolved oxygen, temperature and pH Nitrifying bacteria utilize carbon dioxide as a of the wastewater. Denitrification is effected by carbon source and oxidize ammonia or nitrite factors like absence of oxygen, temperature, pH, to derive energy. Nitrification is carried out by availability of carbon source, nitrate availability, two types of nitrifying organisms. The first hydraulic load and HRT. Nitrogen in wetlands step converts ammonium to nitrite (aerobic can also be removed by nutrient uptake of plants. conditions), and the second converts nitrite to The plants uptake nitrogen in the form of ammo- nitrate. Soil organisms include Nitrosospira, nium or nitrate, which is then stored in the plant Nitrosovibrio, Nitrosolobus, Nitrosococcus in the organic form. The uptake capacity of emer- and Nitrosomonas. The second step converts gent plant species in constructed wetlands can vary nitrite to nitrate and is accomplished by facul- from 200 to 2,500 kg.ha−1 year−1. Factors effect- tative chemolithotrophic bacteria which can ing nutrient uptake of plants is growth rate of utilize organics for cell growth an energy. The plants, concentration of nutrients in the plant tis- only organism found in soil of freshwater sues and climatic conditions. The major portion which oxidizes nitrites is Nitrobacter. Nitrifi of the nitrogen removal is through bacterial con- cation also is influenced by temperature, pH, version as compared to nutrient uptake by plants. alkalinity present and dissolved oxygen. The Major nitrogen transformations occur in a ideal temperature is from 30 to 40 °C. The pH FWS wetland. Bacillus, Micrococcus and values range from 6.6 to 8.8 and proper Pseudomonas are important denitrifying organ- amounts of alkalinity and dissolved oxygen isms in soils, and Pseudomonas, Aeromonas and must be present. Vibrio are important in aquatic environments. In In wetlands, the nitrogen removal process starts the presence of oxygen, the organisms break with the nitrification. It is a two-step process, down organics into carbon dioxide and water. where the nitrogen fixing bacteria takes energy The electron transport system enables the organ- from the process of ammonification and carbon isms to denitrify in anaerobic conditions. Under source to convert nitrogen to different forms (He low oxygen levels, the production of nitrite from et al. 2012). Ammonia ion is oxidized in the pres- ammonia is favoured over nitrate formation from ence of oxygen by Nitrosomonas bacteria. ammonia. There are a variety of wetland plants that can fix nitrogen but the process requires a NH+++®ONOH++2 H 42 2- 2 large amount of cellular energy (Vymazal 2006). Biological removal involves uptake and assimila- The nitrite is then oxidized to nitrate in the tion of nitrogen by wetlands plants that convert absence of oxygen by the nitrobacter bacteria. inorganic nitrogen to organic nitrogen. The assimilated nitrogen is further converted to

22NO --+®ON2 O ammonia and nitrate. Burial of organic nitrogen 2 3 leads to its incorporation into wetland soil. The next step is denitrification, where nitrates FWS wetlands have different ways of removing are reduced to organic N. Denitrification occurs nitrogen than VSB wetlands. Plant uptake is the pri- under anaerobic conditions and in the presence of mary mechanism for reducing nitrogen in FWS organic matter—which is the carbon source. This wetlands. Volatilization also offers large reducer of reaction is catalyzed by Pseudomonas sp. bacte- nitrogen in FWS wetlands. Ammonification gets ria. The N formed from denitrification is released organic nitrogen in the state of ammonia so that it in to the atmosphere in the form of nitrous oxide, can be removed by other processes. Denitrification thereby removing nitrogen from the wetland is the primary mechanism of removing nitrogen in system. wastewater wetlands (Vymazal 2006). Above-ground biomass and total biomass NO +®Co()rganic NC++OHO 3- 222 were significantly correlated with ammonia 4.3 Contaminants Removed by Wetlands 79 nitrogen removal and below-ground biomass with soluble reactive phosphorus removal. In Nitrogen subsurface horizontal flow systems, the oxidized nitrogen is immediately reduced, preventing the enrichment of nitrite and nitrate. Horizontal sub- STEP I surface flow constructed wetlands in the Mediterranean and continental Mediterranean Nitrification region of Spain planted with Phragmites austra- Ammonia lis showed higher ammonium mass removal efficiency in the summer than in the winter. Fibrous-root plants showed significantly greater Aerobic root biomass and a larger root surface area per conditions plant than the rhizomatic-root plants and exhib- Nitrite ited accelerated growth in both shoots and roots compared to the rhizomatic-root plants (Obarska- Pempkowiak and Gajewska 2003, 2004; González-Alcaraz et al. 2012). The wetland Nitrate STEP II microcosms planted with fibrous-root plants showed significantly higher ammonium–nitrogen (NH4–N) and nitrate–nitrogen (NO3–N) removal rates than those planted with the rhi- Denitrification zomatic-root plants. Studies suggested that root characteristics of wetland plants related to root distribution and decontamination ability are crit- Anaerobic conditions ical for selection of wetland plants with a higher Organic N contaminant removal capacity and in the con- struction of a multi-species wetland plant community (Fig. 4.4). Fig. 4.4 Steps involved in nitrogen removal from The hybrid constructed wetlands ensure wetlands more stable removal rates of nitrogen in comparison to one-stage systems. The removal of 4.3.1.3 Phosphorus nitrogen takes place in VF beds and HF beds Wetlands do not provide the direct metabolic (denitrification), but efficiency of nitrogen pathway to remove phosphorus. The major phos- removal by nitrification was limited in VF beds phorus transformation in wetlands is done by in wetland systems. Studies indicate that pilot- physical/chemical/biological means (DeBusk scale and full-scale surface constructed wet- et al. 1996b). Inorganic form, i.e. orthophos- lands remove COD, total suspended solids, phate, is removed by algae and macrophytes. The nitrate and ammonium and hence improve water major uptake is by plant roots (Vymazal 2006). quality of waters (Díaz et al. 2012). Simulated The absorption through leaves and plant parts is vertical flow constructed wetlands (VFCWs) usually very low. The storage of phosphorus in planted with Canna indica showed significant plants varies depending upon plant type and stor- removal of nitrogen (N), ammonium N age occurs preferably in below-ground parts. + (NH4 –N) and phosphorus (P). Lower hydraulic Some amount of chemical transformation through loading rate or longer hydraulic retention time soil adsorption and precipitation is also reported. + (HRT) result in a higher removal of TP, NH4 –N The extent at which phosphorus can be removed and TN because of more contacts and interac- or stored is dependent on the type of wetland. tions among nutrients, substrates and roots Removal mechanism includes sorption, storage under the longer HRT (Cui et al. 2010). in biomass and formation of new soil media 80 4 Role of Wetlands

Death Plant biomass Litterval

Efflux Decomposition Growth, uptake

Leaching Surface water Litter

Inflow Deposition Detrital accretion

Sediments

Fig. 4.5 Phosphorus cycle in wetlands (Sundaravadivel and Vigneswaran 2001)

(Kang 2012). Phosphorus is also released after a from the water is fixed in the matrix of phos- plant dies and begins to decay. The decaying phates and metals. Decomposition of litter plant matter above ground releases phosphorus (dead plants) and organic matter in the wetland into the water while decaying roots secrete phos- also takes up phosphorus. This process results in phorus into the soil. Another important chemical storage of phosphorus in the organic matter transformation is soil adsorption and precipita- which will be released eventually. Growing tion. This process involves soluble inorganic plants take up nutrients like phosphorus, thereby phosphorus moving from the pores in the soil reducing levels in the wetland. The plant uptake media to the soil surface. of phosphates varies from 30 to 150 kg ha−1year−1 Phosphorus is present in the water in the form (Sundaravadivel and Vigneswaran 2001). of orthophosphate and organic phosphorus. It is found in the wetlands as part of sediments. 4.3.1.4 Suspended Solids Phosphorus cycle in wetlands is shown in Suspended solids are removed by two different Fig. 4.5. Adsorption is the most important phos- approaches. Free water surface wetland removes phorus removal process in the wetlands. suspended solids primarily by flocculation/sedi- Adsorption of phosphorus occurs due to reac- mentation and filtration/interception. Both of tions with iron, calcium and magnesium present these processes are influenced by particle size, in sediments. Adsorption of phosphorus to iron shape, specific gravity, and properties of the fluid ions takes places under aerobic and neutral to medium. Flocculant settling involves the acidic conditions to form stable complexes. If the interacting of particles changing size and charac- conditions are anaerobic, adsorption to iron ions teristics. If larger flocculants are formed, then the is less strong. Adsorption to calcium ions takes settling of the new particle will occur faster. FWS place under basic to neutral pH conditions. Thus wetlands can typically see hydraulic loads about adsorption of phosphorus to the ions removes it 0.01 m day−1 to 0.5 m day−1. Smaller particles from the wastewater. Adsorption is reversible would take about 200 days to settle out. Filtration process and each substrate has a particular capac- does not typically play a large part in suspended ity until it cannot absorb any more phosphorus. soils removal of FWS wetlands since the plant Phosphorus can also get precipitated with iron stems of plants are too far apart. Interception and or aluminium ions. Under this process, phosphate adhesion to plant surfaces play an important part 4.3 Contaminants Removed by Wetlands 81 in solid removal. The surfaces of plants in wet- dation. It has been demonstrated that ketoprofen lands are coated with active layer of biofilm can be removed from surface and sea waters called periphyton which can absorb colloidal and through photodegradation processes. soluble matter. These solids may then be metabo- CWs offer as good efficiencies as conven- lized and then converted to gases or biomass. tional WWTPs for the removal of caffeine, Removal of suspended solids in VSB wetlands naproxen, methyl dihydrojasmonate, salicylic depends upon hydraulic design and microbial acid and ibuprofen. This good efficiency of CWs characteristics of the substrate. VSB wetlands are could be related to the coexistence of various effective in removing suspended solids due to microenvironments with different physicochemi- low velocity and large surface area of the media. cal conditions in CWs and ponds, which would VSB wetlands offer gravity settling, straining allow for the degradation of PPCPs following and adsorption onto gravel and plant media (EPA several metabolic pathways. Physicochemical 1999). It has been found that 60–75 % percent of conditions in WWTPs are more homogeneous solids removal in VSB wetland occur in the first and would induce fewer degradation pathways. one third of the wetland. One of the major con- Furthermore, photodegradation processes are cerns with VSB wetlands is the clogging of the easier in ponds and surface flow CWs, since filter media. As suspended solids pass through they are shallower than WWTPs (Hijosa-Valsero the soil media, it can clog pores and reduce the et al. 2010a). hydraulic conductivity of the media producing head losses at the entrance of the wetland (Manios et al. 2003; Wei et al. 2012). In order to stop clog- 4.3.2 Organic Contaminants ging larger particle media (10–15 cm) that offer larger void space and less shear resistance to flow Small-scale constructed wetlands remove organic were chosen. The larger void space also decreased load efficiently (Imfeld et al. 2009; De Biase et al. the surface area for which bacteria to grow, thus 2011; Agudelo et al. 2012; Zhou et al. 2013). helping in proper removal of suspended solids. Physical, chemical and biological processes interact and work in concert during attenuation of 4.3.1.5 PCPPs organic chemicals in wetland systems. The main PPCP removal processes suggested for Degradation pathways work for different groups the systems studied are based on biodegradation, of contaminants. In constructed wetlands, trans- plant exudates and uptake and photodegradation. formation and mineralization of nutrients and Studies indicate that the removal of many PPCPs organic pollutants is facilitated by microorgan- from wastewater is favoured by oxic conditions, isms. The contaminants in the wastewater are since the most feasible biodegradation process metabolized in various ways depending on the of these substances is an aerobic microbiological oxygen input and the availability of other electron pathway. Ibuprofen removal efficiency is favoured acceptors. Uptake of xenobiotics (organic in aerobic environments. Naproxen, salicylic pollutants) by the plants is influenced by several acid, caffeine and methyl dihydrojasmonate physicochemical factors such as the octanol– were more efficiently removed by the wetland water partition coefficient (log KOW), acidity con- with higher redox potential. Nevertheless, some stant (pKa) and concentration (Wenzel et al.

PPCPs like diclofenac are degraded anaerobi- 1999). Compounds with a log KOW between 0.5 cally (Zwiener and Frimmel 2003; Quintana and 3 are taken up best. The metabolism of et al. 2005). The coexistence of aerobic and xenobiotics is divided in plants into three phases: anaerobic conditions in the natural systems transformation, conjugation and compartmental- studied would allow for the degradation of differ- ization (Sandermann 1992). The enzymes involved ent kinds of PPCPs. Andreozzi et al. (2003) and are cytochrome P450, glutathione transferase, Matamoros et al. (2009) have suggested that carboxylesterase, O- and N-glucosyl transferases some PPCPs can also be removed by photodegra- and O- and N-malonyl transferases. After 82 4 Role of Wetlands

Fig. 4.6 Examples of different Organic contaminants categories of organic contaminants

Pharmaceuticals Pesticides

carbamazepine, dichlorodiphenyltrichloroethane (DDT),

naproxen, others-

diclofenac, polycyclic aromatic hydrocarbons (PAH),

ibuprofen, bisphenol A,

caffeine, BTEX,

salicylic acid, glycol,

ketoprofen polychlorinated biphenyls (PCB),

clofibric acid cyanide,

benzene,

chlorophenols

transformation, detoxification occurs via export Organic removal is different for FWS and VSB into the cell vacuole, extracellular space and inte- wetlands. FWS wetlands remove organic matter gration into lignin or other components of the cell by physical means and biological means membrane. In subsurface flow systems, aerobic (Sobolewski 1999). The biofilms located on plant processes only predominate near roots and on the surfaces offer pathways for plants to break down rhizoplane (the surface of the roots). organics. The biological separation processes of In case of chlorinated organic compounds, cor- organics include sorption and volatilization. The responding carbon atoms are attacked by nucleo- main types of reactions involved in organic matter phile rather than oxidative reactions. Highly breakdown and transformation include aerobic, chlorinated hydrocarbons are dehalogenated. The anoxic and anaerobic via respiration, denitrifica- only realistic possibility of biologically degrading tion, acid fermentation, sulphate reduction and hexachlorobenzene perchloroethylene or highly methanogenesis. In an aerobic environment, oxy- chlorinated biphenyls is reductive dehalogena- gen is present and serves as the terminal electron tion. The low-chlorinated products can then acceptor. In an anoxic environment, nitrates, sul- undergo further biological degradation under phates and carbonates serve as the terminal elec- aerobic conditions. The degradation of 4-chloro- tron acceptors which are reduced to form oxides. phenol by a mixed bacterial culture obtained Amount of volatile organic compounds entering from Phalaris arundinacea roots was enhanced wastewater wetlands is fairly low; hence, 80–96 % by the rhizodeposition products. Phenol degra- removal is achieved. The aerobic microorganisms dation chiefly takes place via catechol and consume oxygen to break down organics which further meta-ring cleavage. In Lemna gibba, provides energy, while anaerobic bacteria break phenyl-beta-D-glucopyranoside was identified down organic matter to produce methane. In an as a metabolite of phenol degradation (Barber aerobic environment, oxygen serves as the termi- et al. 1995; Fig. 4.6). nal electron acceptor. In an anoxic environment, 4.3 Contaminants Removed by Wetlands 83 nitrates, sulphates and carbonates serve as the Removal of compounds followed first-order terminal electron acceptors which are reduced to decay kinetics with decay constants higher in the form oxides. Aquatic macrophytes located on top planted beds than the unplanted beds. of the surface of the water play an important role Constructed wetland removed emerging in producing oxygen to the water. Anaerobic contaminants (i.e. pharmaceuticals, sunscreen bacteria break down organic matter to produce compounds, fragrances, antiseptics, fire retardants, methane. Organisms break organics into energy pesticides and plasticizers) efficiently, presum- including oxidation and reduction reactions, ably due to the presence of plants (Phragmites hydrolysis and photolysis. Bacteria, actinomy- and Typha) as well as the higher hydraulic retention cetes and fungi play maybe the most important time (HRT) in the CW (Matamoros et al. 2007, role in breaking down organic matter. Macrophytes 2010, 2012a, b; Zhang et al. 2012a, b). Studies are aquatic plants located on top of the surface demonstrated that aquatic plants contribute of the water which play an important role in directly and indirectly to the aqueous depletion producing oxygen to the water (EPA 1999). of emerging organic pollutants in wetland The mechanism for organic removal in VSB systems through both active and passive pro- wetlands is a little different than in FWS wet- cesses that involved microbial degradation and lands since VSB wetlands function as fixed sorption. Removal of atrazine, meta-N,N-diethyl film bioreactors. The particulate organic material toluamide (DEET), picloram and clofibric entering a VSB wetland undergoes a similar acid and depletion of fluoxetine, ibuprofen, mechanism as suspended solids. The particulate 2,4-dichlorophenoxyacetic acid and triclosan by organic material entering a VSB wetland under- aquatic plants have been reported. Wetlands goes hydrolysis and produce soluble organic reduce concentrations of personal care products matter which enter the media and attach to bio- (PPCPs). Oxygen status may affect the attenua- film media and then further decomposed. The tion of PPCPs in wetland sediments by influenc- amount of decomposition of organic matter is ing microbial activity. Redox conditions, aerobic/ low since average dissolved oxygen concentra- anaerobic conditions and other factors effect tions in a VSB wetland are less than 1 mg L−1. The sorption and degradation of PPCPs. Sorption of predominant biological mechanism for organic PPCPs like N,N-diethyl-meta-toluamide (DEET), removal is done by aerobic/facultative means. carbamazepine and gemfibrozil has been VSB wetlands have strong reducing capabilities reported. Degradation of the selected PPCPs was which make the predominant metabolic mecha- enhanced under aerobic conditions. Studies indi- nism an aerobic manner. Anaerobic functions cated that PPCP removal associated with the dis- include methanogenesis, sulphate reduction and solved phase exhibited a seasonal pattern. In the gentrification which all produce gaseous prod- dissolved phase, the overall removal efficiency in ucts. These functions vary with temperature and summer ranged from 70 to 85 % for salicylic it is possible that as temperatures increase, greater acid (SAL), methyl dihydrojasmonate, caffeine amounts of gas can be released (EPA 1999). (CAF), ketoprofen and triclosan, whereas in winter Mesocosm-scale constructed wetlands showed it declined for most of the PPCPs to between 30 pharmaceutical removal capacity (carbamaze- and 50 %. SF CW generally exhibited the highest pine, naproxen, diclofenac, ibuprofen, caffeine, removal efficiency for most of the contaminants salicylic acid, ketoprofen and clofibric acid) from (Matamoros and Salvadó 2012). synthetic wastewater. Pharmaceutical removal Constructed wetlands mainly VFSSCWs with efficiency was significantly and inversely corre- gravel matrix and a plant-root mat showed lated with log Dow value, but not with log Kow potential for groundwater and surface water value. The horizontal subsurface flow CWs (i) remediation as removal of benzene, aniline, efficiently removed compounds ketoprofen and nitrobenzene, BTEX, MTBE, ammonia-N and salicylic acid; naproxen, ibuprofen and caffeine; gasoline-range organics was achieved. Const- and carbamazepine, diclofenac and clofibric acid. ructed wetlands exhibited capacity for treatment 84 4 Role of Wetlands of domestic wastewater where BOD and COD of pyrethroids and chlorpyrifos from agricultural (biochemical and chemical oxygen demand, runoff water. Chlorinated ethenes (CEs) are respectively) are used as a sum parameter for groundwater contaminants. CEs polluting the organic matter (Seeger et al. 2011; Yada et al. groundwater can be remediated both naturally 2011). Wetlands may be considered as a feasible and cost-effectively by biodegradation in wetland alternative for mitigating emerging contaminants environments. Highly chlorinated CEs, such as from river water. Case studies highlight the tetrachloroethene (PCE), have the potential to treatment of wastewaters contaminated with undergo reductive biodegradation in the reducing aromatic organic compounds and sulphonated environments, and less-chlorinated CEs, such as anthraquinones, olive mill wastewater, landfill trichlorethene (TCE), dichloroethene (DCE) iso- leachate and groundwater contaminated with mers, vinyl chloride (VC), can undergo oxidative hydrocarbons, cyanides and chlorinated volatile. biodegradation both in the near-surface environ- Wetlands planted with Phragmites australis ment and root zone, also called rhizosphere, of showed removal of monochlorobenzene (MCB), wetland plants. Wetland roots provide several 1,4-dichlorobenzene (1,4-DCB) and 1,2-dichlo- potential oxidative pathways for the biodegrada- robenzene (1,2-DCB). Removal efficiency in tion of CEs. The greatest potential is for oxida- the CW generally decreased with depth and tion with oxygen as the electron acceptor, either seasonal variations. Increased contaminant loss co-metabolically or metabolically, which is was found during summer. Removal potential leaked from the roots into the soil. Co-metabolic was attributable to microbial degradation, vola- oxidation of CEs with CH4 as a growth substrate tilization and plant uptake. MCB removal was is highly likely because wetland soil is rich in caused by improved oxygen supply and direct organic matter produce an abundance of CH4 to plant uptake. be used by methanotrophic bacteria inhabiting Engineered treatment system (EETS) showed the root zone. Constructed wetland (at the natural attenuation of estrogenic endocrine Wright-Patterson Air Force Base (WPAFB)) in disrupting compounds (EDCs) such as estriol Dayton exhibited potential for removal of PCE in (E3, natural) and 17α-ethinylestradiol (EE2, syn- the groundwater. PCE degrades in the deeper, thetic) (Kumar et al. 2011). These two estrogens anaerobic portions of treatment wetland, as mea- are the major contaminants of sewage and found sured by its disappearance along with formation to cause adverse effects on the endocrine system of its daughter products (e.g. TCE, DCEs and of humans and animals when exposed even in VC). The daughter CEs appear to readily degrade nanogram concentrations. The EETS consisted at the shallower depths, possibly due to the activ- of diverse biota, namely, aquatic macrophytes, ities associated with the wetland vegetation. The submerged plants, emergent plants, algae and biogeochemical factors affect the oxidative deg- bacteria present in the system mimic the natural radation of daughter CEs. There is a redox cleansing functions of wetlands and help in the gradient in the wetlands with reducing conditions treatment of pollutants present in wastewater. near the bottom and more oxygenated conditions The floating macrophytes system was more effec- near the surface and in the root zone. Oxygenated tive in removing estrogens compared to the conditions and methanotrophic activity in the submerged–emergent macrophyte-based integrated plant rhizosphere support co-metabolic and met- system and submerged–rooted macrophytes abolic aerobic degradation of CEs in the shallow system. On the whole, EETS can effectively treat vegetated wetland. EDCs and remove COD, nitrates and turbidity Wetland species Myriophyllum spicatum and (Cai et al. 2012). Ceratophyllum demersum planted in the aquaria Constructed wetlands (CWs), along with other showed capability of removing textile dye – Basic vegetative systems, help in mitigating pesticides. Blue 41(BB41). Removal of ~90 % is achieved Operational CWs located in the Central Valley of at hydraulic retention times (HRTs) ranging California explored the mechanisms of removal between 3 and 18 days. The studies provided 4.4 Limitations 85 the evidence that wetland system is also able and RDX removal were standardized. Submersed to remove the dye from influent wastewater plants are identified as having the highest (Keskinkan and Göksu 2007). explosives-removing activity. Myriophyllum aquaticum showed potential to transform RDX. 4.3.2.1 Explosives Phytoremediation of explosives or ammunition- 4.3.2.2 Wastewater contaminated water in groundwater using con- Constructed wetlands are an effective and low- structed wetlands is a potentially economical cost way to treat water polluted with inorganic remediation alternative. Use of aquatic and wet- and organic compounds. Industrial wastewater, land plants in constructed wetlands aimed at urban storm water, swine wastewater, domestic removing explosives from water need to be wastewater, olive mill wastewater, groundwater checked for considerations such as (1) plant and landfill leachate contain several different persistence to the exposed levels of explosives, pollutants, including natural organic matter (2) plant weight specific removal rates, (3) plant (NOM), effluent organic matter (EfOM), toxic productivity and (4) fate of parent compounds and anions, nitrate, bromate, perchlorate, pharmaceu- transformation products in water, plants and sedi- tical chemicals, endocrine disrupters aromatic ments. Field demonstration studies at Milan Army organic compounds, sulphonated anthraquinones, Ammunition Plant, Tennessee (1996), demon- hydrocarbons, cyanides, chlorinated volatile strated the feasibility of constructed wetlands for organics and explosives and other micro-pollutants treating contaminated groundwater. Two different (Vymazal and Sveha 2012a, b; Wu et al. 2012). systems, (a) lagoon system planted with sago Constructed wetlands depicted efficacy in treating pondweed, water stargrass, elodea and parrot wastewaters from different sources by removing feather and (b) gravel-bed system planted with metals, total suspended solids, BOD, total canary grass, wool grass, sweet flag and parrot Kjeldahl nitrogen (TKN), dissolved oxygen (DO) feather, were designed and installed. The gravel-bed and conductivity. High sequestration of K, Na, wetland reduced 2,4,6-trinitrotoluene (TNT) and Mg and Ca from municipal wastewater by vege- 2,4,6-trinitrobenzene (TNB) concentrations, while tation in subsurface horizontal flow planted with gravel-bed wetland removed hexahydro-1,3,5- Phragmites australis and Phalaris arundinacea trinitro-1,3,5-triazine (RDX) and octahydro- has been noted. Arundo had higher growth rates 1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX) in and biomass and is a preferred species use in the groundwater. Mass balance studies demon- CWs treating tannery wastewater and hence strated that TNT disappeared completely from decreased the toxicity of the wastewater. groundwater with plants. Highest specific removal rates were found in submersed plants and emergent plants. Growth of submersed plants 4.4 Limitations was normal, but that of emergent plants reduced in groundwater amended with RDX. Highest specific Constructed treatment wetlands have some RDX removal rates were found in submersed limitations as follows: plants in elodea, in emergent plants and in reed • Relatively large area requirements canary grass (Best et al. 2012). Parent compounds • A long starting time period required for and transformation products were analyzed using growth of vegetation 14C analyses. Groundwater and plant tissue analy- • Season and climatic conditions ses indicated that TNT is degraded to reduced by- Studies have shown that CWs are more suit- products and to other metabolites in the presence able for wastewater treatment in tropical than in of the plants. The kinetics predicts that TNT temperate areas, because in a warm climate, there removal was best modelled using first-order kinet- is year-round plant growth and microbiological ics (25 °C). Hydraulic retention times (HRTs) activity, which in general have a positive effect ranging from 4.9 to 19.8 days for TNT degradation on treatment efficiency (Kadlec and Wallace 86 4 Role of Wetlands

2009; Garfí et al. 2012). In cold conditions, CW • Mechanisms of wastewater disinfection. design can be adapted in order to improve wet- • The effect of root growth on hydraulic con- land performance, mainly using lower contami- ductivity should be studied in detail. nant mass loading rates and longer hydraulic • Genetic engineering provides a growing retention times (HRTs) (Akratos et al. 2008; number of methods to breed plants, which Hijosa-Valsero et al. 2010a, b). Other parameters can, for instance, better accumulate heavy that affect wetland performance are influent qual- metals or break down persistent contami- ity and wetland design, such as HRT, plant spe- nants more effectively in constructed wet- cies, primary treatment and feeding pattern lands. However, attention must always be (Hijosa-Valsero et al. 2010a, b; Kotti et al. 2010; paid to how these ‘new’ plant species can Pedescoll et al. 2011; Stefanakis and Tsihrintzis stand up in the long term to the many com- 2012). Biomass disposal problem and seasonal peting influences such as wild species in growth of aquatic macrophytes are some limita- these complex technical ecosystems—just tions in the transfer of phytoremediation technol- as crops in the field permanently have to ogy from the laboratory to the field. Determining compete with weeds. the longevity of treatment wetlands is compli- • Interactions of various substance cycles (e.g. cated by various factors including inflow hydrau- carbon, nitrogen, and sulphur), taking into lic and pollutant loading rates, natural factors account above all the variability of redox such as extreme weather conditions, and the type states in the rhizosphere. of pollutants for which the wetlands are designed. Though, constructed wastewater wetlands Studies related to sustainability of FWS wet- have shown capability of treating different lands for wastewater treatment is still ongoing, kinds of wastewater with capacity for removing particularly for P removal, and long-term records suspended solids, organic matter, nitrogen, provide evidence of the longevity of treatment phosphorus, pathogens and metals. Proper wetlands (Kadlec and Wallace 2009). understanding of mechanisms for removal of contaminants is required for large-scale implementation of wastewater treatment in con- 4.5 Future structed wetlands. Though the utility of wetlands for mass-scale removal of contaminants is well A number of fundamental aspects of exactly how established, a few questions regarding their constructed wetlands function are not yet ade- functioning still need to be addressed. It is quately understood. One reason for this is that, observed that metals taken up by roots are trans- compared to other technologies such as activated ported upwards to above-ground tissues, but the sludge, constructed wetlands depend on the inter- route for their excretion is not clearly defined. action of many more different components (Rai The decomposing litter of plant species will get 2008). enriched with metals over time, which may The basic aspects upon which more work is leach or may become available to detritus essential include the following: feeders. A comprehensive understanding of the • Microbial process of anoxic ammonium oxi- uptake, tolerance and transport of heavy metals dation and possibilities of stimulating it in in the wetland system through aquatic plants constructed wetlands. will be essential for the development of phytore- • Behaviour of toxicologically highly active mediation technologies. trace substances such as persistent drug resi- Achieving a better understanding of the com- dues in the complex system of the constructed plex interactions involved will enable the basic wetland. scientific aspects to be optimally combined with • Removal and detoxification of persistent the technical possibilities available, thus enabling compounds from wastewater in this complex wetland technologies to be used on a broader system. scale. Advances in wetland modelling are 4.5 Future 87 presented as a powerful tool for understanding 2006). Nutrients accumulating in plants may also multiple interactions occurring in subsurface be used for composting or energy generation as flow constructed wetlands during the removal of additional benefits (Cicek et al. 2006). Harvested contaminants. plants can be used for biogas production through Wetlands can be expected to sustain their fermentation, a practice widely used in develop- performance as long as appropriate hydrology ing countries and Europe. A floating mat-based and vegetation are maintained and detritus system (also called floating treatment wetlands) removal occurs regularly. Two FWS wetlands, has been developed and used in the UK, Belgium, the Brillion Marsh in Wisconsin and Great China and other countries. The floating mat- Meadows Marsh in Massachusetts, operated for based system is a variant of the conventional over 70 years and retained their treatment effi- FWS design that employs EAV species growing ciency (Kadlec and Wallace 2009). In contrast, a as a floating mat or raft on the water surface tertiary treatment wetland, the Easterly Wetland instead of rooted plants in the sediments. Because in Orlando, Florida, has reduced 70–80 % of the of this feature, floating treatment wetlands offer a nutrient load, but has showed a slight decline in promise for rainfall-driven storm water treatment nutrient removal efficiency over time. Proper systems because they are less affected by water management is crucial to the sustainability of an level fluctuations. The engineered floating mat- effective FWS system (Carty et al. 2008; based systems, therefore, incorporate EAV spe- Rousseau et al. 2008). Self-sustaining system cies growing in a hydroponic manner on floating may not be possible for FWSCWs where nutri- rafts and enable the incorporation of treatment ent loading and/or sedimentation rates are high wetland elements into deep pond-like systems. and system hydrology is altered seasonally or The multiple linear floating wetlands with syn- for operational and maintenance purposes. thetic textile curtains hanging beneath are used to Maintaining healthy vegetation is also impera- provide additional substrate for biofilm attach- tive to sustaining both effective water quality ment and to create a lengthy flow path (Todd treatment and habitat value. Minimum mainte- et al. 2003). Introducing this floating mat-based nance, including adjustment of flows and water system into a pond-marsh system or a degraded levels, is required to achieve successful perfor- shallow lake has a number of advantages that mance in FWS systems (Carty et al. 2008; may enhance pollutant removal processes or lake Rousseau et al. 2008; Kadlec and Wallace restoration. Like any constructed wetland, FWS- 2009). Wetland design criteria often are not CTWs have limitations. In many cases, overload- reflective of extreme environmental conditions ing or uncontrolled discharging of wastewater such as weather and hydrologic fluctuations may result in an irreversible degradation or fail- (Thullen et al. 2005; Mitsch and Gosselink ure of the system. The buildup of sediment from 2007) that can negatively impact wetland func- wastewater and the accretion of peat from decom- tioning and decrease wetland sustainability. posed vegetation affect the operation of the Design features of the San Joaquin Wildlife CTWs. Over the past several decades, FWS- Sanctuary that provide for the dual purposes of N CTWs have been used extensively throughout removal and the creation of avian habitat do not North America and many are in operation in inhibit removal of total N. A number of other Australia, Asian, and European countries benefits of FWS-CTWs such as the creation of (Ghermandi et al. 2007; Kadlec and Wallace wetland habitat and biodiversity conservation are 2009). Using FWS-CTWs for water quality important for sustainable resource management improvement is cost effective and environmen- (Rousseau et al. 2008; Carty et al. 2008). tally sound. The capabilities of the FWSCTWs in Conserving biodiversity is essential to many eco- water pollutant removal, together with other system services (e.g. biotic regulation and aes- ecological services, provide a nature-based thetic values) in both the wetland and the technology that supports sustainable resource surrounding landscape (Siracusa and La Rosa management. 88 4 Role of Wetlands

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The success of the phytoremediation technology trees with a deep root system (up to 30 ft below depends upon its implementation at different land surface) to facilitate the uptake of contami- sites and a potential to treat/remove various nated groundwater. US Air Force also remediated contaminants. Many fi eld scale, site-specifi c and TCE from groundwater using poplar trees. pilot scale studies have been conducted, though Numerous defence sites across the USA including remediation conditions are different for each con- Milan Army Ammunition Plant had groundwater taminant (Pilon-Smits 2005 ; Salt et al. 1998 ). contaminated with explosives like TNT, RDX, Selection of the most effi cient plant species to octahydro-1,3,5,7-tetranitro-1,3,5,7-tetraazocine degrade a particular compound is the most impor- (HMX) and DNT. These contaminants have been tant determining step in this technology. successfully treated using constructed wetlands. The rate of remediation of any contaminant Plant nitroreductase enzyme is able to degrade depends on selection of plant species which is TNT, RDX and HMX. Remediation of soils con- climatically adapted with desired growth charac- taminated with PAHs have been achieved using teristics. A plant with good root system is effec- plant species Medicago sativa (alfalfa), Panicum tive as increased root mass increase the surface virgatum (switch grass) and Schizachyrium sco- area available for microbial colonization and root parium grass (little bluestem). Myriophyllum exudation, hence facilitating higher contaminant aquaticum has been successfully used in the removal from the soil. Increased microbial num- remediation of soils contaminated with TNT as bers in rhizosphere zone enhance microbial deg- well as other organic contaminants such as TCE. radation of contaminant. The plant has also shown potential for phytotrans- Technique has been successfully implemented formation of perchlorate (Susarla et al. 2002 ). at many sites, but till date most of the success stories have been related terrestrial plants. Trees of the Salicaceae family (willow and poplar) have 5.1 Limitations been used at several locations in phytoremedia- of Phytoremediation tion technology because of their fl ood tolerance Technology and fast growth. Ecolotree™ reported application of phytoremediation of organic contaminants Like any other technology, phytoremediation, such as trichloroethylene using poplars. Poplar besides possessing a number of positive points trees possess extensive root systems that act as that makes it widely acceptable, have certain lim- pump to draw water from deepwater tables and itations. Some of them are listed below: transpire the water back to the atmosphere. A 1. It is generally considered as a time-consuming proprietary technique, called TreeMediation™, process and may take at least several growing also has been developed that uses hybrid poplar seasons to clean up a site. For example, in

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 95 DOI 10.1007/978-81-322-1307-9_5, © Springer India 2013 96 5 Future Prospects

one estimate considering the slow growth 8. Effi cacy for phytoremediation varies for rate and biomass production, remediation of species or varieties. There can be a wide metals could not be achieved even within range in their response to a contaminant and 10–20 years (Ernst 1996 ). Another estimate concentration of that contaminant, in their suggests that treatment of heavy-metal- uptake or metabolism of the contaminant or contaminated site using Thlaspi caerulescens in their ability to grow under specifi c soil and would require 13–14 years to be remediated climatic conditions. (Salt et al. 1998 ). Therefore, selection of 9. Site-specifi c studies may always be neces- faster growing plants and hyperaccumulators sary prior to implementation. becomes a prerequisite. 10. Growth of vegetation requires great care due 2. Intermediates formed from organic and inor- to abiotic and biotic stresses such as climate ganic contaminants may be cytotoxic to plants. and pests. Additions to or modifi cations of 3. Excavation and disposal or incineration of normal agronomic practices might be contaminated plant matter takes weeks to required and may have to be determined months to accomplish. Harvesting and through greenhouse or pilot scale tests. proper disposal are regulatory requirements 11. It might require use of a greater land area for plant biomass that accumulates heavy than other remedial methods. metals or radionuclides (Adler 1996 ). 12. Amendments and cultivation practices might 4. Risk analysis for human and other ecological have unintended consequences on contami- receptors given the potential pathways for nant mobility. For example, application of contaminant transformation and transfer is many common ammonium-containing fertil- also required. Potential risk of horizontal izers can lower the soil pH, which might gene transfer to related wild or cultivated result in increased metal mobility and leach- plants is an important barrier associated with ing of metals to ground water. Potential development of transgenic plants for effects of soil amendments should be under- bioremediation. stood before their use. 5. Depth of plant root is also a main factor that 13. Nature and extent of contamination, hydro- affects the plant’s potential for uptake. logical and geological characteristics and Selection of deep-rooted plants and the use site characteristics must be assessed. of techniques to induce deep rooting could help alleviate this disadvantage. 6. Performance of remedial technology is 5.2 Enhancement affected by climatic conditions and other of Phytoremediation biotic factors. Technology can lose its effec- Effi ciency tiveness during winter (when plant growth slows or stops) or when damage occurs to the Due to limitations of phytoremediation such as vegetation from weather, disease or pests. low biomass of hyperaccumulator species, plant 7. Transfer of toxic contaminants to various sensitivity to high concentrations of environmen- components of food chain or bioconcentra- tal pollutants as well as other abiotic stresses and tion of toxic contaminants by components of less effi ciency of ions and compounds which food chain and environment is an issue of have low bioavailability to uptake by plants, major concern, especially if there is transfor- several approaches have been explored to enhance mation of the contaminant results into a the effi ciency of this technology (Reeves and more toxic, mobile or bioavailable form. Baker 1999 ). Although chemicals (e.g. surfac- Sampling and analysis of the aboveground tants and ligands) can increase phytoextraction, plant matter and degradation products may phytodegradation or phytostimulation effi ciency be necessary to ensure that the contaminants of pollutants through enhancement of bioavail- are not transferred to the food chain. ability of organic and inorganic compounds in 5.2 Enhancement of Phytoremediation Effi ciency 97 media, nature-based methods like using plant– growth, root surface area and development of microorganisms symbiosis seem to be more lateral roots (Dimkpa et al. 2009 ). acceptable because of less side effects, hence According to Kang et al. (2010 ), ACC protecting food chain. Plant symbiosis with fungi synthesized in plant tissues by ACC synthase and bacteria have been tried to get increase in is thought to be exuded from plant roots and phytoremediation effi ciency of various environ- be taken up by neighbouring bacteria. mental pollutants. Subsequently, the bacteria hydrolyze ACC to The various approaches used for enhancing ammonia and 2-oxobutanoate. This ACC phytoremediation potential have been discussed hydrolysis maintains ACC concentrations low below: in bacteria and permits continuous ACC transfer from plant roots to bacteria. Otherwise, ethylene can be produced from ACC and then 5.2.1 Plant–Bacteria Symbiosis cause stress responses including growth inhibition. Rhizospheric bacteria have shown benefi cial 2. Inoculation with nonpathogenic rhizobacteria effects on various plants and were named as plant can induce signalling cascades and plant sys- growth-promoting rhizobacteria (PGPR). They temic resistance; alter the selectivity for Na, K are categorized into two types: extracellular and and Ca ions resulting in higher K/Na ratios; intracellular PGPR (Dimkpa et al. 2009 ). The and change in membrane phospholipid con- latter group includes bacteria which are capable tent as well as the saturation pattern of lipids of entering the plant as endophytic bacteria and (Dimkpa et al. 2009 ). are able to create nodules, whereas extracellular 3. Bacteria may produce osmolytes, such as gly- PGPR are found in the rhizosphere and rhizo- cine betaine, and act synergistically with plant plane or within the apoplast of the root cortex, osmolytes, accelerating osmotic adjustment but not inside the cells (Dimkpa et al. 2009 ; (Dimkpa et al. 2009 ). Rajkumar et al. 2009 ). Plant-associated bacteria 4. PGPR containing 1-aminocyclopropane- 1- can promote plant growth as well as reduce and/ carboxylic acid (ACC) deaminase activity or control of environmental stresses which reduces ethylene level within the plant and together affect phytoremediation effi ciency consequently facilitates plant growth under through several approaches directly and indi- stress conditions (Dimkpa et al. 2009 ; Kang rectly, within the plant and/or in the rhizosphere et al. 2010 ). (Dimkpa et al. 2009 ; Rajkumar et al. 2009 ; Yang Rhizosphere play a role in abiotic stress toler- et al. 2009 ; Glick 2010 ; Kang et al. 2010 ). A ance by performing different roles. These include: number of soil microorganisms are capable of (1) Nitrogen fi xation by rhizobacteria positively degrading xenobiotic compounds and conse- infl uence host plant growth by increasing nitrogen quently reduce their related stress to plants in availability (Dimkpa et al. 2009 ; Kang et al. 2010 ; contaminated soils (Glick 2010 ). Several mecha- Rajkumar et al. 2009 ). Therefore, they can act as a nisms that induce abiotic stress tolerance within biofertilizer which affect plant growth. (2) the plant or in the rhizosphere include: Rhizobacteria reduce the mobility of heavy metals 1. Production of phytohormones (e.g. auxins, in contaminated soils in root zone bacteria which cytokinins, gibberellins) which can change fi nally cause precipitation of metals as insoluble root morphology is an adaptation mechanism compounds in soil and sorption to cell components of plant species exposed to environmental or intracellular sequestration. (3) Bacterial migra- stresses (Dimkpa et al. 2009 ; Weyens et al. tion from the rhizoplane to the rhizosphere reduce 2009 ). Indole acetic acid as a subgroup of plant uptake of metals (e.g. Cd). (4) Iron- chelating auxins together with nitric oxide is produced siderophores complexes can be taken up by the in plant shoot transported to root tips and host plant, resulting in higher fi tness (Dimkpa consequently enhance cell elongation, root et al. 2009). They can also form complexes with 98 5 Future Prospects other nonsoluble metals (e.g. Pb), enhancing their which can also be important to reduce heavy ability to uptake by hyperaccumulators such as metal stress in plants (Schützendübel and Polle Brassica napus. (5) Rhizosphere bacteria infl uence 2002 ). pH and redox potential in the rhizosphere through the release of organic acids. This increases avail- 5.2.2.1 Endophytic Fungi ability of nutrients (e.g. phosphorous) for the Endophytes induce mechanisms of drought plant. (6) PGPR can act as biocontrol agents which avoidance (morphological adaptations), drought mitigate the effect of pathogenic organisms tolerance (physiological and biochemical adapta- (Dimkpa et al. 2009 ; Rajkumar et al. 2009 ). tions) and drought recovery in infected grasses (Malinowski and Belesky 2000 ). Aluminium toxicity mainly in acidic soils can be reduced on root 5.2.2 Plant–Fungi Symbiosis surface of endophyte-infected plants through Al sequestration which appears to be related to exu- Arbuscular mycorrhizal fungi (AMF) that are dation of phenolic-like compounds with naturally present in the roots of most plant spe- Al-chelating activity (Malinowski and Belesky cies form a mutualistic association. Endophytic 2000). Besides, drought and light stress as well as fungi live systemically within the aerial portion salt stress could be reduced in endophyte-infected of many grass species and help in improving plants via release of some proteins (e.g. dehy- plant tolerance to biotic and abiotic stresses drins) and phenolic-like compounds in the rhizo- (Hildebrandt et al. 2007 ; Lingua et al. 2008 ; sphere (Kuldau and Bacon 2008 ; Malinowski and Soleimani et al. 2010a ). These fungi reduce Belesky 2000 ). Endophytic fungi positively abiotic stress by regulating oxidative stress (by affect phytoremediation of heavy metals as well reducing the amount of malondialdehyde) as organic pollutants such as petroleum hydrocar- (Bressano et al. 2010 ). AMF are useful for phy- bons (Soleimani et al. 2010a , b ). toremediation, especially in metal-contaminated soils (Bressano et al. 2010 ; Jiang et al. 2008 ; Lingua et al. 2008). Mycorrhizal fungi in association 5.2.3 Biotechnological Approach with poplars are suitable for phytoremediation purposes (Lingua et al. 2008 ). Furthermore, some The use of transgenic plants for phytoremediation fungi have the potential to degrade organic applications has been studied extensively. pollutants via extracellular or intracellular Transgenic plants have been produced for phy- oxidation using various enzymes, such as lac- toremediation of both heavy metals and organic case, peroxidase, nitroreductase and transferases pollutants ( Macek et al. 2000 , 2008 ; van Aken (Harms et al. 2011), and thereafter reduce stress 2009 ; van Aken et al. 2010 ). Genetic transforma- of organic compounds in soil. AMF reduce metal tion of plants for enhanced phytoremediation stress in host plants and improve plant growth capabilities is achieved by introduction of exter- and development via production and excretion nal genes whose products are involved in various of organic acids (e.g. citrate and oxalate) detoxifi cation processes. The genes for metabolic which increase dissolution of primary minerals enzymes from microbes and mammals have been such as phosphate (Harms et al. 2011 ), release of introduced to achieve a near-complete mineral- siderophores can enhance iron uptake by plant ization of organic molecules in plants. Genes and boost the growth. Extra-hyphal immobiliza- isolated from various plant, bacterial and animal tion may occur through the complexation of met- sources that can enhance metal accumulation or als by glomalin (i.e. metal-sorbing glycoproteins degradation of organics is desired (Newman excreted by AMF) and biosorption to cell wall et al. 1997 ; Dhanker et al. 2002 ). These changes constituents such as chitin and chitosan will include transformation of plants to add spe- (Harms et al. 2011 ). Metallothionein is another cifi c proteins or peptides for binding and trans- protein excreted by some mycorrhizal fungi porting xenobiotics, increasing the quantity and 5.2 Enhancement of Phytoremediation Effi ciency 99 activity of plant biodegradative enzymes (peroxi- neering Festuca for improved metal tolerance and dases, laccases, oxygenases, dehalogenases, or accumulation. Transformation of plants using nitroreductases, nitrilases), including those that modifi ed bacterial merA gene ( mer A9) for are exported into the rhizosphere and surround- detoxifying Hg (II) has been the most successful ing soil to improve the performance of soil bacte- approach till date. Several plant species including ria. Introduction of foreign genes might be Arabidopsis , tobacco, poplar, rice, Eastern cotton- responsible for the synthesis of low-molecular- wood, peanut, salt marsh grass and Chlorella have weight organic molecules to be excreted in exu- been transformed with these genes. The merA dates, such as some phenolics, fl avonoids or gene codes for a mercuric ion reductase that coumarins, that induce rhizospheric bacteria to removes Hg from stable thiol salts by reducing it degrade anthropogenic toxins. Transgenic plants to volatile metallic Hg. Mercuric reductase has with genes for microbial biodegradation can be also been successfully transferred to Brassica, created. Transgenic approach targets the genes tobacco and yellow poplar trees (Pilon-Smits responsible for overexpression or knockdown of et al. 1999 ). merA or merB genes have been membrane transporter proteins to enhance expressed in plants via nuclear or chloroplast uptake, accumulation and/or degradation of vari- genome, expressing organomercurial lyase and/or ous contaminants. Genetic engineering of plants mercuric ion reductase in the cytoplasm, endoplas- by insertion of genes allowed metabolism of mic reticulum or within the plastids. Salt marsh TCE, chlorinated hydrocarbons, phenolics and cordgrass (Spartina alternifl ora ) modifi ed for Hg herbicides. phytoremediation showed resistance up to 500 μM

Molecular biology techniques will facilitate HgCl2. Plants tend to accumulate most mercury in formation of plants with improvement in phy- roots, and translocation to shoot tends to be a toremediation technology. This can be done by major limitation; therefore, an ability to express developing plants specifi cally for enhanced metal membrane proteins, transport proteins and translo- accumulation and degradation of organics by cators could further enhance mercury phytoreme- transforming plants by adding specifi c proteins diation capabilities. The recent research focuses or peptides for binding and transporting xenobi- on expression of membrane proteins transforming otics, increasing the quantity and activity of plant the chloroplast genome with mer transporters to biodegradative enzymes (peroxidases, laccases, enhance Hg accumulation. Alternatively, the merC oxygenases, dehalogenases, nitroreductases, can be coupled to a chelator gene like poly- nitrilases). Introduction of foreign genes include phosphate kinase (ppk ) or metallothionein (mt ), to those responsible for the synthesis of low- develop transgenic plants that could accumulate molecular-weight organic molecules (phenolics, Hg (Ruiz and Daniell 2009 ). fl avonoids or coumarins) to be excreted in exu- Expression of a yeast metallothionein gene for dates that induce rhizospheric bacteria to degrade higher Cd tolerance in tobacco plants, overex- anthropogenic toxins. pression of a Zn transporter protein in Arabidopsis thaliana for higher Zn accumulation in roots are 5.2.3.1 Metals few examples of use of biotechnological approach Genes for higher tolerance and accumulation of for achieving high phytoremediation potential contaminants such as heavy metals have been (Meagher et al. 2000 ). Genes for heavy metal expressed. The V Framework Research Program resistance and uptake such as AtNramps (Thomine of the European Community includes two projects et al. 2000 ); AtPcrs (Song et al. 2004 ); CAD1 on the production of genetically modifi ed plants from Arabidopsis thaliana , library enriched in Cd- for phytoremediation, PHYTAC and metallo- induced cDNAs from Datura innoxia (Louie phytes. PHYTAC aims to transfer genes from et al. 2003 ); gshI , gshII (Zhu et al. 1999a ); and PCS the hyperaccumulator Thlaspi caerulescens to cDNA clone (Heiss et al. 2003) from Brassica the high-biomass-producing Brassica or tobacco, juncea (Zhu et al. 1999b ) have been isolated and while the metallophytes project is devoted to engi- introduced into plants. Other transgenic raised 100 5 Future Prospects include A. thaliana tolerant to Al, Cu and Na with herbicides (Karavangeli et al. 2005 ), organomer- gene Glutathione S-transferase from tobacco curials (Bizily et al. 2000 ), phenolic compounds (Ezaki et al. 2000 ); tobacco with Ni tolerance (Wang et al. 2004 ), PCBs (Mohammadi et al. and Pb accumulation with gene Nt CBP4 from 2007 ) and nitroaromatics (Hannink et al. 2001 ; tobacco; tobacco and rice (Goto et al. 1998 , Rylott et al. 2006 ). 1999) with increased iron accumulation with Many plant enzymes appear to play important gene Ferretin from soybean; A. thaliana and roles in xenobiotic degradation, including mono- tobacco resistant to Hg with gene merA from bac- and dioxygenases, dehydrogenases, hydrolases, teria (Rugh et al. 2000 ; Bizily et al. 2000 ; Eapen peroxidases, nitroreductases, nitrilases, deha- and D’Souza 2005 ); Indian mustard tolerant to logenases, phosphatases and carboxylesterases Se transformed with a bacterial glutathione (Dietz and Schnoor 2001 ; Singer et al. 2003 ; reductase in the cytoplasm and also in the chloro- Pilon-Smits 2005 ). Biotechnologists are using plast (D’Souza et al. 2000 ); and transgenic A. potential of these enzymes to increase the reme- thaliana plants expressing SRSIp/ArsC and ACT diation ability of suitable plant species. Some of 2p/γ-ECS together showed high tolerance to As. these enzymes appear to be naturally released into the soil, where they are capable of degrading 5.2.3.2 PCBs organic pollutants ranging from solvents to Transgenic plants and associated bacteria treat explosives (Singer et al. 2003 ). The reactions polychlorinated biphenyls (PCBs)-contaminated catalyzed by plant P450s extend from simple soil and water in an effi cient and environmental- hydroxylation or epoxidation steps to more com- friendly way (Mackova et al. 1997 , 2007 ). plex phenol coupling, ring formation and modifi - Organic contaminants including PCBs are slowly cation or decarboxylation of appropriate taken up and degraded by plants and associated substrates. Helianthus tuberosus CYP76B1 and bacteria because of their hydrophobicity and soybean (Glycine max (L) Merr.) CYP71A10 chemical stability, resulting in incomplete treat- were the fi rst plant enzymes shown to actively ment and potential release of toxic metabolites metabolize a herbicide (Robineau et al. 1998 ; into the environment. In order to overcome these Siminszky et al. 1999 ). Since then, several plant limitations, bacterial genes involved in the P450s have been associated with the degradation metabolism of PCBs, such as biphenyl dioxygen- of relevant organochemicals, including several ases, have been introduced into higher plants, POPs. However, most P450s expressed heterolo- following a transgenic approach. Bacterial gously in plants for remediation purposes are of biphenyl dioxygenases produce cis -diol inter- mammalian origin. Human cytochrome P450 mediates susceptible to ring cleavage and com- gene CYP2E1has been expressed in tobacco to plete mineralization. Francova et al. ( 2003 ) get enhanced metabolism of trichloroethylene genetically modifi ed tobacco plants (Nicotiana (Campos et al. 2008 ). The expression of mam- tobacum ) by insertion of the gene responsible for malian cytochrome P450 genes in transgenic 2,3-dihydroxybiphenyl ring cleavage, bph C, potatoes and rice plants has been used to detoxify from the PCB degrader Comamonas testosteroni . herbicides. Rice plants transformed with genes Mohammadi et al. (2007 ) inserted bph genes from encoding human cytochrome P450 genes B. xenovorans LB400 into tobacco plants. CYP1A1, CYP2B6 and/or CYP2C19 showed more tolerance to various herbicides including 5.2.3.3 Herbicides and Explosives atrazine, metolachlor and norfl urazon. Transgenic Studies have also been conducted to develop rice plants carrying CYP1A1 show herbicide tol- plants with an increased ability to degrade explo- erance towards atrazine, chlorotoluron, diuron, sives such as GTN and TNT by overexpressing a quizalofop-ethyl and other herbicides, and they bacterial NADPH-dependent nitroreductase. reduce the levels of atrazine and simazine in Other successful experiments with genetically hydroponic solutions. Transgenic rice carrying modifi ed plants have tackled contamination by CYP2B6 germinate well in medium containing 5.3 Cost Analysis 101 chloroacetanilide herbicides, such as alachlor, aquatic ecosystems or in constructed wetlands to metolachlor and thenylchlor. Transgenic plants clean up Hg or Se pollution. overexpressing detoxifying enzymes such as Practical application in case of genetically laccase 1 (LAC1) showed higher capacity for modifi ed organisms requires a thorough study of degrading herbicides in rhizosphere (Kawahigashi ecological, social and legal issues. The potential et al. 2005a , b , 2007; Kawahigashi 2009 ). impact of transgenic plants on the target habitat Transgenic plants that produce a root-specifi c and the fate of the introduced gene also need to laccase (LAC1) to the rhizosphere have shown be studied. The potential of transgenic plants enhanced resistance to a variety of phenolic needs to be further validated to know the effi - allelochemicals and to 2,4,6-trichlorophenol. ciency of this technique for cleanup of contami- Overexpression of glutathione transferases nated sites and their integration into sustainable (GSTs) genes enhances the potential for phytore- cropping and management systems. mediation of herbicides. Introduction of this gene into poplar plants leads to higher concentrations of glutathione, and the plants show tolerance 5.3 Cost Analysis towards two chloroacetanilide herbicides, aceto- chlor and metolachlor. Indian mustard ( Brassica Environmental pollution is a global problem with juncea) expressing this gene shows increased tol- cleanup costs running into billions of dollars erance to atrazine, 1-chloro-2,4-dinitrobenzene using current engineering technologies. The (CDNB), metolachlor and phenanthrene. Maize availability of alternative, cheap and effective GSTs are known to detoxify triazine and chloro- technologies would signifi cantly improve the acetanilide herbicides, and transgenic tobacco prospects of cleaning up contaminated sites. plants expressing maize GST I have been shown Phytoremediation has been proposed as an eco- to remediate alachlor. Transgenic alfalfa, tobacco nomical and ‘green’ method of treating contami- and Arabidopsis plants expressing a bacterial nated sites. Economic outlook is an important atrazine chlorohydrolase (atzA) gene show consideration for any technology to be practically enhanced metabolic activity against atrazine implementable. This mainly includes capital (Flocco et al. 2004 ; Karavangeli et al. 2005 ; investment required for its operation and mainte- Kawahigashi 2009 ). nance. Phytoremediation is an emerging technol- In context of aquatic plants, genetic engineer- ogy; standard cost information still is being ing of high-biomass-producing, fast-growing developed on the basis of experiences in imple- aquatic plants with an enhanced capacity to accu- menting phytoremediation projects. mulate metals and degrade xenobiotics plants is These cost considerations for the implementa- desirable. Genetic engineering studies for devel- tion of phytoremediation can be divided into four opment of transgenic wetland species such as primary categories: Spartina sp., Typha sp. and S cirpus sp. by inser- 1. Design tion of the Mer genes are in progress. The wet- 2. Installation land species Scirpus maritimus and Typha 3. Operation and maintenance latifolia have shown the accumulation of toxic 4. Sampling and analysis heavy metals such as Se that is facilitated by 1. Design considerations include feasibility plant–bacteria interactions at the root interface, studies, plant selection and the associated as well as further transformation by bacteria to engineering costs. Green house studies or organic form, which can be further excluded by pilot scale testing may be needed to determine methionine biosynthetic pathway or converted to which plants to use and assess the possibility volatile form that can escape into atmosphere of phytoremediation as a treatment option for (Dhir et al. 2009 ). These prospective transgenic the site. The salaries of manpower performing wetland plants, namely, Scirpus maritimus and conceptual work for the site will be the domi- Typha latifolia , can be planted in contaminated nant cost in the design phase. 102 5 Future Prospects

2. Installation costs include site preparation, process, from growing, maintaining and harvest- soil preparation, materials and labour. This ing plants to disposing or recycling the metals in includes clearing or levelling land/soil followed the plants. The consensus cost of phytoremedia- by soil preparation that involves pH adjust- tion has been estimated at $25–$100 per ton of ment, nutrient addition or tilling. Site prepara- soil treatment and $0.60–$6.00 per 1,000 gal for tions require labour and materials including treatment of aqueous waste streams. According to equipment, organic matter, irrigation systems, 1997 US EPA estimates, the cost of using phy- plant stock and vector protection materials toremediation in the form of an alternative cover for the plants. (vegetative cap) ranges from $10,000 to $30,000 3. Operation and maintenance (O&M) costs will per acre, which is thought to be two- to fi vefold include monitoring equipment, power sources, less expensive than traditional methods. The maintenance for the equipment and labour. expenses of phytoremediation represent less than 4. Sampling and analysis costs will depend half of the price needed for any other effective upon length of the project as monitoring is treatment. required and data analysis is required at Phytotech, Inc. reports that cleanup costs, frequent intervals. Costs include labour or including treatment and disposal, can range from machinery to collect samples and lab work $20 to $80 per cubic yard of contaminated soil fees associated with analyzing samples. Data (Linacre et al. 2005). The cost estimate given collected during sampling and analysis is includes incineration of plants and ash disposal at crucial for thorough documentation of site a hazardous waste incinerator at a cost of $500 progress and the performance of technology. per cubic yard of material. If the plants can be This may dominate the overall cost of the recycled at a smelter, costs near the low end of project due to the length of time. the range can be expected. The costs of cleanup Phytoremediation costs will vary depending of various heavy metals at the Twin Cities Army on the treatment strategy. Though phytoreme- Ammunition Plant Project, Minneapolis, St. diation is often predicted to be cheaper Paul, MN, were reported in the Federal than comparable technologies, still, costs of Remediation Technologies Roundtable to be phytoremediation are highly site specifi c. For $153 per cubic yard of soil over the life of the example, harvesting plants that bioaccumu- project. The costs of removing radionuclides late metals can drive up the cost of treatment from water with sunfl owers have been estimated when compared to treatments that do not to be $2–$6 per 1,000 gal of water (Dushenkov require harvesting. et al. 1997 ). Costs of cleanup of explosives at the Cost comparisons of phytoremediation to other Milan Army Ammunition Plant, Milan, TN, were remediation technologies have recently been reported in the Federal Remediation Technologies made. The cost of phytoremediation for 1 acre of Roundtable (see Supporting Resources) to be sandy loam soil to a depth of 50 cm is estimated to $1.78 per 1,000 gal of water over the life of the range from $60,000 to $100,000. This is consider- project. Estimated costs for hydraulic control of ably lower than the approximate cost of $400,000 an unspecifi ed contaminant in a 20-foot-deep for excavation and disposal of the contaminated aquifer at a 1-acre site were $660,000 for conven- soil at the landfi ll. The cost of plant disposal can tional pump and treat and $250,000 for phytore- be signifi cantly less than the cost of disposal of mediation (EPA/600/R-99/107). Studies indicate metal-contaminated soils because contaminants that phytoremediation is competitive with other have been concentrated in the much smaller plant treatment alternatives, as costs are approximately biomass. However, the total cost of phytoremedi- 50–80 % of the costs associated with physical, ation will depend on the rates of uptake from the chemical or thermal techniques at applicable soil and the number of crops which are needed to sites (Thomas et al. 2003 ). Some more actuarial meet cleanup levels. Analysis of the costs of phy- studies need to be carried out to give an estimate toremediation must include the entire remedial of the perceived costs of remediation works that 5.4 Conclusions and Future Developments 103

Estimates of phytoremediation costs versus costs of established technologies (USEPA 2000 ) Contaminant Phytoremediation costs Estimated cost using other technologies Metals $80 per cubic yard $250 per cubic yard Site contaminated with petroleum $70,000 $850,000 hydrocarbons 10 acres of lead-contaminated land $500,000 $12 million Radionuclides in surface water $2–$6 per 1,000 gal None listed treated 1 ha to 15 cm depth (various contaminants) $2,500–$15,000 None listed

Ecolotree Inc.’s cost estimates of a poplar tree phytoremediation system (USEPA 2000 ) Activity Cost Installation of trees at 1,450 trees/acre $12,000–$15,000 Predesign $15,000 Design $25,000 Site Visit $5,000 Soil cover and amendments $5,000 Transportation to site $2.14/mile Operation and maintenance $1,500/acre with irrigation $1,000/acre without irrigation Pruning $500 Harvest $2,500 Court esy: http://clu-in.org/products/intern/phytotce.htm#1

will be useful for project sanctioning authorities a longer period of time at sites where phytoreme- or decision-makers. diation is used. According to laboratory, pilot scale work and fi eld information costs associated with these four categories are relatively small in 5.4 Conclusions and Future phytoremediation in comparison to traditional Developments remediation technologies. The primary factor in cost reduction is the energy source of the Phytoremediation is fast becoming recognized as operating systems. Traditional systems utilize a cost-effective method for remediating sites con- electric power, at a substantial cost, to pump taminated with toxic metals, radionuclides and water, while phytoremediation systems take hazardous organics at a fraction of the cost of advantage of free solar energy. Moreover, conventional technology. Phytoremediation is phytoremediation is in situ and requires no predicted to account for approximately 10–15 % digging or hauling of contaminated soil. Apart of the growing environmental remediation mar- from this, little or no mechanical equipment ket by the year 2010. Research related to this is required to operate the phytoremediation relatively new technology needs to be promoted process. Individual sites will vary in cost and emphasized and expanded in developing regardless of the technology being applied. In countries. In addition, environmental aesthetics contrast, monitoring costs could be higher should not be ignored. Under phytoextraction, than with conventional treatment technologies the cost of processing and ultimate disposal of because monitoring typically is required for biomass generated is likely to account for a major 104 5 Future Prospects percentage of overall costs (USEPA 2000 ). The Dushenkov S, Kaplunik Y, Fleisher DKC, Ensley B (1997) use of plant roots as ‘biocurtains’ or ‘biofi lters’ for Removal of uranium from water using terrestrial plants. 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Dr. Bhupinder Dhir has been working as a for developing eco-friendly wastewater technology scientist at University of Delhi South Campus, by using aquatic plant biomass. Strong research India, since last 5 years. Her academic background background in the relevant area provides her a is related to botany. Main research interests are in specialization and expertise in the development subject areas such as plant physiology, stress of phytoremediation technology. The quality of physiology, ecology and environment. The main research is reﬂ ected in research articles published focus of her research is on environmental stress in journals of national and international repute. responses in plants and development of strategies She has 22 research publications to her credit.

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 107 DOI 10.1007/978-81-322-1307-9, © Springer India 2013 Index

A Constructed wetlands , 17, 19, 31–32, 37–40, 55, 65–70, Adsorption , 5, 8, 9, 13, 14, 27–31, 35, 39, 52, 58, 59, 67, 73–77, 79, 81, 83–87, 95, 101 70–74, 76, 77, 79–81 Contaminants , 1–6, 8–18, 21–41, 51–62, 65–68, 70–87, Algae , 5, 6, 8–9, 70, 79, 84 95, 96, 99, 100, 102–104 AMF. See Arbuscular mycorrhizal fungi (AMF) Copper , 3, 4, 9, 11–14, 22, 23, 26, 28–31, 33–35, 37–41, Ammonia , 4, 9, 31, 77–79, 84, 97 53, 71–77, 100 Anthropogenic , 1, 3, 4, 99 Cyanide , 4, 17, 38, 57, 58, 65, 71 Arbuscular mycorrhizal fungi (AMF) , 98 Arsenic (As) , 3, 7, 12, 13, 16, 22, 23, 26–29, 31–33, 35, 37–41, 53, 54, 67, 71, 72, 74, D 75, 100 Dichloro diphenyl trichloroethane (DDT) , 3, 7, 8, 16, 25, Aspergillus , 7, 8 27, 37, 59, 60 Azolla , 18, 25, 29–30 Domestic , 1, 4, 5, 8, 26, 28, 29, 38, 40, 65–67, 71, 84, 85 Duckweeds , 18, 21, 24–27, 58, 74

B Bacillus , 7, 8, 78 E Bacteria , 4–8, 14, 27, 30, 40, 53, 55, 56, 62, 68, 70, EDCs. See Endocrine disrupting chemicals (EDCs) 72–74, 76–78, 81, 83, 84, 97–101 Eichhornia crassipes , 13, 21, 22, 25, 27–29, 55, 68, Bioaccumulation , 7, 8, 10, 17, 25, 26, 51, 54, 60 73–76 Biochemical oxygen demand (BOD) , 1, 26, 29, 31, Elodea , 18, 21, 36–37, 59, 85 38–40, 71, 84, 85 Emergent plants , 18, 21, 36, 37, 52, 62, 74, 77, 78, 84, 85 Biodegradation , 6, 8, 14, 30, 33, 35, 37, 60, 67, 71, 81, Emerging pollutants , 83 84, 99 Endocrine disrupting chemicals (EDCs) , 2, 3, 84 Biomagniﬁ cation , 3, 60 Environment , 1–6, 14–16, 26, 27, 30, 34, 51, 68, 73, 74, Bioremediation , 6–10, 96 77, 78, 81–84, 96, 100 Biosorption , 7, 9, 27, 29, 31, 35, 51, 98 Enzymes , 4, 7–8, 11, 15, 26, 28, 30, 34, 36, 37, 54, Biotechnology , 98–101 56–62, 73, 75, 76, 81–82, 95, 98–101 BOD. See Biochemical oxygen demand (BOD) Explosives , 3, 10, 18–19, 21, 23, 24, 26, 27, 34, 37, 57–58, 61–62, 65, 69, 85, 95, 100–102

C Cadmium , 3, 4, 9, 11–14, 16, 17, 22, 23, 26–41, 53, 66, F 71–76, 97, 99 Free-ﬂ oating , 24–32 Carcinogens , 3 Freshwater wetlands , 76 Ceratophyllum , 32–33 Fungi , 5–8, 14, 56, 57, 73, 83, 97, 98 Chemical oxygen demand (COD) , 1, 29–31, 33, 39, 40, 68, 71, 79, 84 Chlamydomonas , 7 G Chloride , 4, 53, 58, 59 Groundwater , 4, 7, 10, 12–18, 21, 31, 34, 37, 61, 62, 66, Chlorinated solvents , 2, 3, 10, 12, 15, 18, 23, 57, 59 69, 74, 83–85, 95, 104 Chromium , 3, 4, 6, 7, 11–14, 16, 20, 22, 23, 28, 29, 31, 32, 35, 38, 40, 41, 74, 77 Cobalt , 3, 9, 11, 13, 23, 31, 35, 66, 71, 74 H COD. See Chemical oxygen demand (COD) Heavy metals , 4, 7, 9, 11, 15, 22, 23, 26–29, 31, 34, Conjugation , 57–58, 60, 81 52–54, 96, 98, 99

B. Dhir, Phytoremediation: Role of Aquatic Plants in Environmental Clean-Up, 109 DOI 10.1007/978-81-322-1307-9, © Springer India 2013 110 Index

Herbicides , 8, 16, 25, 27, 37, 61, 100 O Horizontal wetlands , 68 Organic , 1, 21, 51, 65, 95 Hormones , 1, 2, 40 Oxidoreductases , 7 Hybrid fl ow wetlands , 68 Oxygenases , 7, 57, 60–62, 99 Hydrilla , 23, 33, 35–36, 68, 73 Hydrocarbons , 2, 3, 6, 8–10, 12, 14, 16, 18, 21–23, 29, 30, 40, 61, 82, 84, 85, 98, 99, 103 P Hydrophobic , 27, 36, 40, 56, 57, 60, 61 Passive uptake , 34, 51, 56 Hyperaccumulators , 11–13, 28, 32, 53, 96, 99 PCPs. See Personal care products (PCPs) Penicillium , 7 Persistent organic pollutants (POPs) , 3, 59 I Personal care products (PCPs) , 3, 15, 65, 83 Industrial , 1, 3–5, 10, 17, 26–31, 35, 38–40, 66, 85 Pesticides , 1–4, 6, 8, 10, 12, 15–17, 26, 27, 30, 37, 39, Inorganic , 1, 3–7, 9–12, 14, 15, 18, 21–23, 25, 26, 40, 56–58, 60, 65, 67, 83, 84 28–40, 51–55, 65, 67, 70–81, 85, 96 Petroleum hydrocarbons , 2, 12, 14, 30, 61, 98, 103 Insecticides , 36 Phanerochaete , 7, 8 Ions , 4, 5, 7, 9, 27, 29, 31, 51, 53, 55, 59, 72, 75, Pharmaceuticals , 2–4, 23, 28, 39, 65, 83, 85 78, 99 Phosphorus , 4, 8, 23, 28, 32, 37–39, 55, 66, 71, 74, Iron , 3, 7, 37, 52, 72–76, 80, 97, 98, 100 79–80, 86 Phragmites , 12, 18, 21, 23, 31, 36, 39, 40, 55, 68, 69, 73, 76, 77, 79, 83–85 L Phyto-volatilization , 11, 12, 14, 18, 61, 70 Laccases , 7, 15, 57–59, 61, 62, 98, 99, 101 Phytoaccumulation , 11 Landfi ll , 10, 17, 40, 65, 66, 84, 85, 102 Phytodegradation , 11, 12, 15, 18, 70, 96 Lead , 3, 4, 6, 11, 17, 26, 31, 32, 38, 39, 57, 66, 72, 76, Phytoextraction , 11–12, 17, 18, 51, 60, 75, 96, 103 78, 101, 103 Phytohormones , 97 Lemna , 12, 18, 21, 22, 24–26, 55, 68, 69, 74, 82 Phytostabilization , 11–14, 16, 18, 51, 75 Phytostimulation , 96 Pistia stratiotes , 21, 22, 30–31, 73 M Polychlorinated biphenyls (PCB) , 3, 5, 8, 10, 15, 34, 36, Macrophytes , 18, 19, 21–23, 27, 31, 51, 52, 55, 61, 67, 59–61, 100 68, 70, 72–74, 77, 79, 83, 84, 86 Polycyclic aromatic hydrocarbons (PAH) , 2, 3, 8, 10, 14, Manganese (Mn) , 3, 11, 13, 14, 21, 23, 31, 33, 35, 16, 17, 61, 95 37–40, 52, 66, 71, 72, 74, 75, 102 POPs. See Persistent organic pollutants (POPs) Mechanism , 6, 7, 9, 11, 27, 28, 31, 34–36, 38, Populus , 15, 16, 57 51–62, 67, 70–72, 75, 76, 78, 79, 83, 84, Potamogeton , 18, 21, 23–25, 32–34, 69, 73, 75 86, 97, 98 Pseudomonas , 7, 8, 73, 78 Mercury (Hg) , 3, 4, 6, 7, 9, 11, 12, 14, 22, 23, 26, 28, 29, 33–35, 39–41, 53, 99, 100, 101 Metals , 3, 21, 51, 65, 96 R Microbes , 1, 5–7, 11, 13, 30, 31, 38, 60, 66, 74, 98 Radionuclides , 3, 4, 6, 7, 9–12, 14, 17, 18, 21, 24, 26, 51, Mine drainage , 3, 73, 74 54–55, 71, 96, 102, 103 Municipal , 1, 4, 5, 10, 17, 26, 28, 33, 38, 40, 66, 85 Removal , 5, 21, 51, 66, 95 Myriophyllum , 15, 18, 21, 23–25, 32–35, 57, 61, 62, 68, Rhizodegradation , 11, 12, 14–16, 18, 70 73, 74, 84, 85, 95 Rhizofi ltration , 11, 12, 14, 18, 38 Rhizosphere , 7, 11, 12, 14, 15, 27, 31, 37, 38, 52, 56, 57, 60, 65, 66, 69–73, 75–77, 84, 86, 95, N 97–99, 101 Neurotoxins , 3 Nickel (Ni) , 3, 9, 11–14, 16, 22, 23, 26, 28, 29, 31–33, 35, 36, 38, 40, 41, 53, 66, 71–74, 76, 100 S Nitrate , 4, 9, 18, 26, 28, 31, 33, 39, 55, 65, 70, 77–79, Salvinia , 18, 21, 22, 25, 31–32, 55, 73 82–85 Scirpus , 12, 18, 21, 23–25, 36, 39–40, 67–69, 74, 101 Nitrite , 4, 31, 72, 77–79 Sequestration , 7, 11, 14, 16, 36, 51, 53, 56–60, 62, 73, Nitrogen , 4, 6, 8, 23, 28, 29, 31–33, 38–40, 55, 66, 68, 75, 77, 85, 97, 98 70, 71, 73, 77–79, 85, 86, 97 Sewage , 1, 3, 10, 26, 28, 31, 38, 66, 84 Nutrients , 8, 24, 26, 28, 30–34, 51, 53, 55, 65, 68, 70, 78, Spirodela , 13, 18, 21, 22, 25, 27, 58 87, 102 Sterols , 1, 2, 14 Index 111

Submerged , 18, 21, 23, 31–35, 39, 51, 52, 55, 62, 67, 68, V 73, 75, 84 Vertical wetlands , 68 Sulphate , 4, 7, 9, 26, 27, 37, 67, 69, 72–74, 76, 77, 82, 83 Volatile organic compounds (VOCs) , 2, 3, 82, 85 Suspended solids , 1, 26, 28, 38–40, 66, 70–73, 79–81, 83, 85, 86 Symbiosis , 97–98 W Wastewaters , 1–6, 8–10, 12, 14, 16–19, 21, 26–33, 35, 36, 38–40, 65–71, 74, 78, 80–87 T Water , 1, 21, 51, 65, 95 Thlaspi , 12, 13, 15, 16, 96, 99 Wetlands , 17–19, 21, 29, 31–34, 37–40, 55, 58, 65–87, Total organic carbon (TOC) , 1 95, 101 Toxicity , 3, 4, 15, 30, 34, 36, 38, 53, 54, 61, 67, 74, 85, 98 Transgenic , 96, 98–101 X Translocation , 10, 11, 28, 31, 36, 52, 53, 55, 56, 73, Xenobiotics , 3, 8, 56, 58, 61, 70, 81, 101 75–77, 99 Transport , 4, 11, 14, 31, 36–38, 51–55, 57, 58, 72, 73, 75, 78, 86, 99 Z Typha , 12, 18, 21, 23, 24, 31, 34, 36–40, 67–70, 73, 74, Zinc , 3, 4, 9, 11–14, 16, 22, 23, 26, 28–31, 33–40, 76, 77, 83, 101 53–54, 66, 71–74, 76–77, 99

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