Phytorestoration of Abandoned Mining and Oil Drilling Sites 9780128212004, 0128212004

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Phytorestoration of Abandoned Mining and Oil Drilling Sites

Phytorestoration of Abandoned Mining and Oil Drilling Sites

Edited by Kuldeep Bauddh

Department of Environmental Sciences, Central University of Jharkhand, Ranchi, India

John Korstad

Oral Roberts University, Tulsa, OK, United States

Pallavi Sharma

Department of Life Sciences, Central University of Jharkhand, Ranchi, India

Elsevier Radarweg 29, PO Box 211, 1000 AE Amsterdam, Netherlands The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States © 2021 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-821200-4 For information on all Elsevier publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Candice Janco Acquisitions Editor: Marisa LaFleur Editorial Project Manager: Alice Grant Production Project Manager: Joy Christel Neumarin Honest Thangiah Cover Designer: Miles Hitchen Typeset by SPi Global, India

Dedication Dedicated to my wife Sweta and daughter Aashwita. Kuldeep Bauddh Dedicated to my wonderful and blessed wife of 48 years, and our 4 beautiful daughters, 4 sons-in-law, and 10 amazing grandchildren. Proverbs 31:10-31 and Psalm 127:3-5. John Korstad Dedicated to my mother Mrs. Geeta Sharma and daughter Adya Jha. Pallavi Sharma

Contributors Joseph Acker  Oral Roberts University, Tulsa, OK, United States Muhammad Aqeel Ashraf  School of Environmental Studies, China University of Geosciences (Wuhan), Wuhan, P. R. China Sneha Bandyopadhyay  Ecological Restoration Laboratory, Department of Environmental Science & Engineering, Indian Institute of Technology (Indian School of Mines), Dhanbad, India Kuldeep Bauddh  Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India Corne Beneke  Oral Roberts University, Tulsa, OK, United States Poulomi Chakravarty  Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India R.P. Choudhary  Department of Mining Engineering, Faculty of Engineering, Jai Narain Vyas University, Jodhpur, India Mary Claire Cooperrider  Oral Roberts University, Tulsa, OK, United States Bhupinder Dhir  School of Sciences, Indira Gandhi National Open University, New Delhi, India R.S. Dubey  Department of Biochemistry, Faculty of Science, Banaras Hindu University, Varanasi; Central University of Gujarat, Gandhinagar, India Elena-Luisa Iatan  Department of Endogene Processes, Natural Hazards and Risk, Institute of Geodynamics “Sabba S. Stefanescu” of Romanian Academy, Bucharest, Romania Sakinatu Issaka  School of Environmental Studies, China University of Geosciences (Wuhan), Wuhan, P. R. China A.B. Jha  Department of Plant Sciences, Crop Development Centre, University of Saskatchewan, Saskatoon, SK, Canada John Korstad  Department of Biology and Global Environmental Sustainability, Oral Roberts University, Tulsa, OK, United States Manoj Kumar  Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India Mukesh Kumar  School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India Alka Kumari  Department of Botany, University of Lucknow, Lucknow, India Khushbu Kumari  Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India

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Contributors Elizabeth J. Lam  Chemical Engineering Department, Universidad Católica del Norte, Antofagasta, Chile Subodh Kumar Maiti  Ecological Restoration Laboratory, Department of Environmental Science & Engineering, Indian Institute of Technology (Indian School of Mines), Dhanbad, India T. Mohan Manu  Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, India Ítalo L. Montofré  Mining Business School, ENM; Metallurgical and Mining Engineering Department, Universidad Católica del Norte, Antofagasta, Chile Sangeeta Mukhopadhyay  Environmental Management Division, CSIR—Central Institute of Mining and Fuel Research (CIMFR), Dhanbad, Jharkhand, India Lakshmi Pathak  Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, India Deepak Kumar Patra  Department of Botany, Nimapara Autonomous College, Nimapara, Puri, India Hemanta Kumar Patra  Department of Botany, Utkal University, Bhubaneswar, India Leandro Santos Peixouto  Instituto Federal de Educação, Ciência e Tecnologia Baiano – IF Baiano, campus Guanambi, BA, Brazil Yslai Silva Peixouto  Instituto Federal de Educação, Ciência e Tecnologia Baiano – IF Baiano, campus Guanambi, BA, Brazil Alanna Cibelle Fernandes Pereira  Centro Universitário FG – UniFG, Guanambi, BA, Brazil Chinmay Pradhan  Department of Botany, Utkal University, Bhubaneswar, India Nopi Stiyati Prihatini  Department of Environmental Engineering, Lambung Mangkurat University, Banjarbaru, Indonesia Sierra Pruitt  Oral Roberts University, Tulsa, OK, United States Yendery Ramírez  Chemical Engineering Department, Universidad Católica del Norte, Antofagasta, Chile; School of Engineering Science, Lappeenranta-Lahti University of Technology, Lappeenranta, Finland Shelby Reiser  Oral Roberts University, Tulsa, OK, United States Vaniele Souza Ribeiro  Instituto Federal de Educação, Ciência e Tecnologia Baiano – IF Baiano, campus Guanambi, BA, Brazil Madhumita Roy  Department of Microbiology, Bose Institute, Kankurgachi, Kolkata, India Lala Saha  Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India Kavita Shah  Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, India Pallavi Sharma  Department of Life Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India Tilak Raj Sharma  ICAR-Indian Institute of Agricultural Biotechnology, Ranchi, Jharkhand, India V. Sheoran  Department of Zoology, Faculty of Science, Jai Narain Vyas University, Jodhpur, India Anil Kumar Singh  ICAR-Indian Institute of Agricultural Biotechnology, Ranchi, Jharkhand, India

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Contributors Lal Singh  Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, India Shipra Singh  School of Environmental Sciences, Jawaharlal Nehru University, New Delhi, India Ragini Sinha  ICAR-Indian Institute of Agricultural Biotechnology; Department of Life Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India Soemarno  Department of Soil Sciences, University Brawijaya, Malang, Indonesia Prafulla Soni  Forest Research Institute, Dehradun, India Sanjog T. Thul  Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, India Jaya Tiwari  Department of Environmental Studies, Zakir Husain Delhi College, University of Delhi, Delhi, India

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Acknowledgment The authors made the challenging assignment to complete this dream a reality by their kind contribution and cooperation. I would like to acknowledge and thank each one of the authors for their contributions whose work, research, and support helped to formulate this book. I express my deep sense of gratitude to the coeditors of the book Prof. John Korstad and Dr. Pallavi Sharma. I take the opportunity to acknowledge the service of the team of Elsevier Publishing and everyone who collaborated in producing this book. Kuldeep Bauddh

This book was a “labor of love” from the beginning—meaning that it was a challenging assignment in terms of time expenditure for each of us when we were already busy with our regular jobs, but we were (and still are) passionate about the need to explain and encourage best practices for sustainable mining and oil drilling globally. I am especially encouraged by the contribution of some of my students as chapter authors in this book who are just beginning their academic careers. They have a bright future ahead! John Korstad

I would like to acknowledge the commitment and professionalism of our contributing authors, coeditors, and publishing team. I am also thankful to my family, friends, and colleagues for their support. Pallavi Sharma

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CHAPTE R 1

Phytoremediation: A sustainable method for cleaning up the contaminated sites Jaya Tiwaria, Poulomi Chakravartyb, Pallavi Sharmac, Ragini Sinhad, Manoj Kumarb, and Kuldeep Bauddhb a

Department of Environmental Studies, Zakir Husain Delhi College, University of Delhi, Delhi, India Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India c Department of Life Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India dICAR-Indian Institute of Agricultural Biotechnology, Ranchi, Jharkhand, India b

1.1 Introduction Sustainability is the only way for the survival of our planet Earth. The current human population of 7.8 billion as of January 2020, is exuding pressure on the limited area and natural resources of the Earth. Higher population results in higher consumption, as well as higher pollution. Pollution is spreading like an epidemic across the world because of recalcitrant nature of contaminants and their vast amount has been a cause of concern in this century (Glick, 2003, 2010). Furthermore, soil contamination with various organic and inorganic pollutants has become a critical global environmental problem with serious implications on public health (Salomons et al., 1995; El-Shahawi et al., 2010). Industrial activities, extraction of natural resources, burning of fossil fuels are some of the major sources of environmental pollution. Mining is another important sector that adds contributes a huge amount of heavy metals (HMs), metal leachates, acids, etc., to the soil, air, and water. The land near the mining areas becomes barren and lay unattended for several years. Similarly, oil drilling sites have various organic contaminants especially hydrocarbons which are considered as wasteland. Various techniques have been tried and employed over the years to curb the ever-increasing menace of contamination. The removal of contaminants from soil is a complex and expensive process. Most of the available physiochemical remediation technologies are either expensive or they demand a huge amount of chemicals and/or energy. There are some technologies that alter the actual characteristics of the soil like soil fertility, microbial diversity, etc. (Khalid et al., 2017; Shah and Daverey, 2020). Often these changes are irreversible for example, in vitrification method soil zone is treated with high temperature Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00019-4 © 2021 Elsevier Inc. All rights reserved.

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4  Chapter 1 (>  1500°C), at such that soil melts and once the soil cools down HMs are entrapped in a glassy matrix. Similarly, during the soil washing, various organic solvents (e.g., sulfuric acid, hydrochloric acid, phosphoric acid, etc.) are utilized to solubilize and mobilize HMs, which adversely affect the soil biology (Liu et al., 2018). Such treated soil is not fit to grow plants and cannot be used for agriculture purposes. One important aspect of soil remediation is that it is also location-specific. Results obtained from a technique in one site may not be transferred to other sites where the type of soil and contaminants are different. Furthermore, if the contaminated soil contains a mixture of organic and inorganic contaminants, the remediation becomes even more complex, owing to different properties of the contaminants and their possible interactions (Reddy and Cameselle, 2009). Phytoremediation was proposed as the most sustainable and benign tool that can deal with mixed contamination (US EPA, 2001). Phytoremediation is a process in which green plants are used for the accumulation, degradation, or stabilization of the contaminants. It is a novel technology that improves the biological quality of soil (Bauddh et al., 2017; Chakravarty et al., 2017; Pandey and Bauddh, 2018; Patra et al., 2020). The remediation technology is used to decontaminate several toxic heavy metals, inorganic and organic pollutants present in the soil, sediments, wastewater, rivers, groundwater, or atmosphere by using wild or genetically modified plants are known as phytoremediation. The phytoremediation techniques have been in use since 1990s (Garbisu and Alkorta, 2001; Campos et al., 2008). Phytoremediation technique has gained much importance in recent years, but despite several efforts in the last 20–30 years on removal of contamination from the soil a huge research gap was felt due to scattered information on phytoremediation. Cultivation of suitable plant species on the abandoned mine and oil drilling sites is found natural and cost-effective method for the reclamation of these sites. After the extensive efforts of several authors, the scattered knowledge on phytoremediation was amalgamated in order to bridge the research gap. Keeping this in view the present chapter focuses on the fundamental mechanism of various phytoremediation techniques for the removal of inorganic and organic contaminants along with its associated advantages and limitations.

1.2  Environmental contamination Any substance that is present in the environment in excess to the original amount can be termed as pollutant. Pollutants can be completely new compounds produced directly from the source as a primary pollutant, as well as that are produced as byproducts of primary one (Manisalidis et al., 2020). The diverse nature of contaminants is the reason for difficulty in categorization of pollutants and thus in effective management too. The wastes generated from industries, agricultural lands, towns, power plants are the general sources of pollution. Although there are various types of contaminants,

Phytoremediation 5 Environmental contaminants Inorganic Heavy metals

Salts

Miscellaneous

Organic Acids

Pesticides

Oil and grease

Solvents

Dyes

Metal nanoparticles

Radio nucleides

Fig. 1.1 Types of environmental contaminants.

some contaminants are potentially more troublemaking than others, Fig. 1.1. Several organic pollutants are persistent in the atmosphere and toxic in nature. The organic xenobiotics are also known as persistent organic pollutants (POPs) as they have a high residence time in the environment. The synthetic organic pollutants include wastes from pharmaceutical industries, pesticides, petroleum wastes, polychlorinated biphenyls (PCBs), and polyaromatic hydrocarbons (PAHs) (Abhilash and Singh, 2009; Kumar et al., 2019). Algal bloom due to the presence of high amounts of fertilizer in agricultural runoff is the cause for the reduction in dissolved oxygen in water bodies which leads to the death of marine life. HMs are another type of pollutants which are naturally present and are also released in the environment by anthropogenic activities. The HM dust, sewage sludge, and leachates are hazardous when they travel far distances and pollute the land air or water (Gaur and Adholeya, 2004). Arsenic, lead, mercury, and cadmium are few of the toxic metals that are harmful to floral and faunal species. Radioactive elements are also determinant to the environment and can cause hazardous effects to health of organism and pollute the surrounding land, water, and air. Radioactive substances are more harmful because of their long residence time in the environment.

1.3  Sources of HMs There are several inorganic and organic pollutants in various components of the environment. Widespread problem associated with toxicity of HMs has received a paramount attention from the researchers globally. As we can easily make out from Fig. 1.2, that we have myriad sources of HMs, which could be both natural and anthropogenic but finally end up in different components of the environment (e.g., lithosphere, hydrosphere, atmosphere, and biosphere). This section discusses various sources of HMs under the following categories.

6  Chapter 1

Fig. 1.2 Potential sources of HMs.

1.3.1  Natural sources of HMs Many prior studies have extensively documented different natural sources of HMs. HMs s are found naturally under different and certain environmental conditions. These natural emissions are volcanic eruptions, sea-salt sprays, fires in forests, weathering of ultramafic rocks, biogenic sources, and air-borne soil particles. Natural weathering processes are responsible for the mobilization of HMs from their native spheres to different environmental compartments. The common HMs are nickel (Ni), chromium (Cr), mercury (Hg), lead (Pb), cadmium (Cd), zinc (Zn), arsenic (As), and copper (Cu). Although the aforementioned HMs are present in traces, but they still are harmful for the growth of plants and serious health implications in humans and other mammals (Herawati et al., 2000).

1.3.2  Anthropogenic processes The release of pollutants in various components of the environment are mainly observed through various anthropogenic processes such as industrial, agricultural, domestic, wastewater, mining, and metallurgical. Furthermore, anthropogenic processes for the release of HMs have been observed to go beyond the natural fluxes for some metals. Metals emitted in wind-blown dusts are mostly from industrial areas. Some important anthropogenic sources which significantly contribute to the HM contamination in the environment include automobile exhaust which is responsible for the emission of lead; smelting which emits arsenic, copper, and zinc; insecticides which release arsenic and burning of fossil fuels emits nickel, vanadium, mercury, selenium, and tin.

Phytoremediation 7

1.4  Toxicity of HMs 1.4.1  Toxicity to plants Adverse effects of HM toxicity on plants are visible through many symptoms, such as low biomass production, chlorosis, growth and photosynthesis inhibition, senescence, perturbed nutrient assimilation, and water balance, which result in plant injury, reduced growth, and even death. HMs influence plant physiology by promoting or inhibiting their growth. Some metals that are required in high concentration have a substantial role in the structural or osmotic activity, while those required at low concentration may indicate their role as a cofactor for specific enzymes. Certain HMs like Fe, Co, Cu, Mo, Mn, and Ni are elements essential for basic metabolisms of plants. However, beyond a certain concentration, these metals inhibit the biochemical processes of plants (as reviewed by Fernandes and Henriques, 1991; Sarma and Sarma, 2007; Sarma et al., 2009). To begin with, many metals affect photosynthetic pigments which, eventually affect the plant’s tolerance ability (Vajpayee et al., 2001). In general, metals cause a reduction in fluorescence associated with chlorophyll (Atal et al., 1991; El-Sheekh, 1992). Atriplex halimus subsp. schweinfurthii, hyperaccumulator of Cd, shows decreased chlorophyll pigments and stomatal transpiration rate and lower root hydraulic conductivity due to high Cd concentration (Nedjimi and Daoud, 2009). Also, the uptake of Cr affects pigmentation and amino acid content in aquatic plants. Vajpayee et al. (2000) showed inhibition of δ-amino laevulinic acid dehydratase by Cr (VI). Cr led carotenoid degradation has been observed in some plants which are metal and plant-specific (Barcelo et al., 1986). In other examples, Hg toxicity has been reported where mercuric cation shows a higher affinity for sulphydryl (-SH) groups, that bind to two sites of protein molecule causing subsequent precipitation of protein (Clarkson, 1972). Therefore, Hg influences light as well as dark reactions of photosynthesis, inhibiting electron transport activity, chlorophyll fluorescence quenching in photosystem II and oxygen evolution. Maximum damage is caused due to the replacement of Mg by Hg that prevents light reaction and ultimately collapse of photosynthesis (Krupa and Baszynski, 1995). Similarly, specific ligands are present on cell membranes that preferentially bind with Hg. Inside the cell, Hg blocks functional groups of enzymes, utilizes transport systems for nutrient ions, denatures enzymes, and disrupts the integrity of cell and organelle membrane (Ochiai, 1987). Thus, Hg toxicity happens due to change in membrane permeability, reaction with sulfhydryl groups and phosphate groups (ADP or ATP), and cation replacements (Kabata-Pendias and Pendias, 1989). In excess amounts, metals like Cu and Fe can be dangerous because they participate in redox cycles and generate hydroxyl radicals which are very harmful to living cells (Stohs and Bagchi, 1995). Cd which is a non-redox metal is strongly phytotoxic and leads to growth inhibition and plant death. It induces alterations in lipid profile (Ouariti et al., 1997) and affects the activities of enzymes such as H+-ATPase which are associated with membranes (Fodor et al., 1995).

8  Chapter 1 It also damages the photosynthetic apparatus (Siedlecka and Baszynsky, 1993), reduces chlorophyll content, and impedes the stomatal regulations (Barcelo and Poschenrieder, 1990).

1.4.2  Toxicity to animals Inappropriate disposal of e-waste, uncontrolled industrial activities, urban runoff from municipal solid and liquid waste, agricultural runoff, burning of fossil fuels, e.g., coal, etc., end up into the aquatic ecosystem either through direct input or precipitation, or weathering or erosion, etc. Thus, there are all the possibilities for aquatic animals of getting exposed to a higher concentration of HMs and causing toxicity (Idrees et al., 2020). Due to the long persistent nature of HMs, they can easily contaminate the food chains and thereafter, the entire ecosystem. As the concentration of HMs gets magnified at each trophic level, the top consumers of a food chain (e.g., human beings) are considered as most vulnerable to exhibit the severe adverse effects. Chronic exposure of HMs may decrease the activities of the central nervous system. It may damage the functioning of various organ systems like pulmonary, hepatic, renal, haematic etc. which may cause muscular dystrophy, Alzheimer’s disease, different types of cancers, and multiple sclerosis (El-Kady and Abdel-Wahhab, 2018). However, the adverse effects caused due to exposure of different HMs, it largely depends on its route of exposure. For example, oral ingestion, inhalation, and dermal contact are perceived as three noteworthy routes of exposure, which also depends upon the type and concentration of HMs (Vardhan et al., 2020). Therefore, in the light of above-discussed problem associated with the toxicity of HMs in plants, as well as animals it is imperative to develop some environmentally sustainable treatment strategies to decrease the HMs load from various components of the environment.

1.5  Remedial measures (traditional measures) As contamination of polluted sites is a common problem throughout the world, several measures for remedy and removal of contaminants are applied. Some of the techniques that are most commonly used to clean the contaminated sites are listed below.

1.5.1  Soil washing Soil washing is an onsite method of contamination removal where two processes are applied; (a) contaminated soil is washed by chemical solvents to remove contamination and (b) concentrating the contaminants by attrition scrubbing, gravity separation, and particle size separation to reduce the size of the contaminants. Radionuclides, HMs, and organic pollutants can be removed with this technique although the process is not cost-effective and a high amount of contaminant laden residue is left which requires further treatment (Tangahu et al., 2011).

Phytoremediation 9

1.5.2  Soil excavation In this process, the contaminated soil is excavated and dumped in another location, which is not a feasible or effective method as it merely dislocates the contaminants to another site (Tangahu et al., 2011).

1.5.3  Electrokinetic treatment This is also an onsite treatment technique where electrodes are used to apply electric potential to contaminated soil and through this process the contaminants migrate toward electrodes by two processes, electromigration and electroosmosis (Cameselle et al., 2013).

1.5.4 Stabilization/solidification In this process a stabilizing agent is utilized to bind the contaminants in the soil (Gomes, 2012). In another method heat is applied to the contaminants to melt them and then solidify them. This process is termed as vitrification.

1.6 Phytoremediation Phytoremediation is the application of plant or plant-based technologies to remediate the contaminated sites (Fig. 1.3). Methods such as chemical reduction/oxidation and incineration are also applied to contaminated sites. The traditional methods have feasibility issue due to expenses, disposal of residues and destruction of soil microflora and fauna. Therefore, researchers are applying innovative techniques to control the contaminants along with maintaining the physical, chemical and biological equilibrium of the sites. Several plants have been investigated to have feasibility to grow in the contaminated sites and bear substantial efficiency to accumulate the toxic substances. These plants can be utilized to remediate the contaminated sites. Different phytoremediator plants have different metabolism and, thereby, the process of contaminant removal may be varied from plant to plant. Some plants can accumulate toxic substance in their roots but restrict the translocation in to their aerial parts. However, other plants have significant efficiency to transfer the toxicants in the shoots. Some common mechanisms of phytoremediation have been discussed as follows.

1.6.1 Phytoextraction In areas of low to medium contamination where the contaminants are present at a shallow depth phytoextraction is a very efficient and cost-effective process (Kumar et al., 1995a, 1995b; Blaylock and Huang, 2000). The roots of the plant extract the contaminants from the medium and then they are translocated to other parts of the plant. The process is beneficial

10  Chapter 1

Fig. 1.3 Mechanism and different aspects of phytoremediation.

as the contaminated metals can be extracted from the ash of the aerial parts of the plants after they are burnt as fuel (Prasad and De Freitas, 2003; Erakhrumen and Agbontalor, 2007; Moreno et al., 2008).

1.6.2 Phytostabilization Some plants have capability to retain contaminants from soil or water medium and keep them stabilized in their tissues, this process is known as phytostabilization. The contaminants are contained by adsorption on surface or precipitation to other parts within the root zone (Prasad and De Freitas, 2003; Erakhrumen and Agbontalor, 2007; Moreno et al., 2008). For the process of phytostabilization to be successful, the plants have to be fast growing with well-developed roots and aerial parts, also need to be tolerant toward external stresses (Ismail, 2012).

1.6.3 Phytovolatilization In the phytovolatilization process, the plants absorb contaminants along with moisture, then accumulate and transfer them into aerial parts, from where they are released into the atmosphere by transpiration (Prasad and De Freitas, 2003; Erakhrumen and Agbontalor, 2007; Moreno et al., 2008). The disadvantage of this process is the return of the toxic volatile contaminants with rainfall and wider spread of the contaminants (Henry, 2000).

Phytoremediation 11

1.6.4 Rhizofiltration Domestic greywater and effluents can be treated applying rhizofiltration method where plants are grown in constructed wetlands and they absorb and accumulate or adsorb and precipitate contaminants in their roots (Prasad and De Freitas, 2003; Erakhrumen and Agbontalor, 2007; Moreno et al., 2008). The plants efficient in rhizofiltration require extensive fast-growing root systems and capacity to accumulate contaminants over a long period of time (Flathman and Hannza, 1998).

1.6.5 Phytodegradation Several studies have confirmed that the organic contaminants can be removed with the help of plants and this process is commonly popularized as phytodegradation (Newman and Reynolds, 2004; Peng et al., 2006; Wang et al., 2008; Vafaei et al., 2012; Zazouli et al., 2014). The plant can remove organic compounds from water, air or soil. Phytodegradation can be done as the degradation of compounds in the rhizospheric region of plants or within the plant body, volatilization after accumulation of compounds (Newman and Reynolds, 2004). Organic contaminants which can be degraded by the plants include explosives, synthetic pesticides, petroleum hydrocarbons (especially poly-aromatic hydrocarbons), solvents, dyes etc. Several plants species like Erythrina crista-galli, Azolla filiculoides, Brassica, Phaseolus vulgaris, Sorghum bicolor, Phragmites australis etc. have been identified to bear potential to degrade the above-mentioned contaminants present in the soil and water ecosystems (Fig. 1.4).

Fig. 1.4 Phytodegradation of organic contaminants (Garrison et al., 2000; Newman and Reynolds, 2004; de Farias et al., 2009; Zazouli et al., 2014; He et al., 2017).

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1.7  Mechanisms of phytoremediation Plants accumulate essential elements along with other components from their growing medium. Non-essential substances especially contaminants are also be absorbed through the same process and channels. The researchers have also reported that several plants behave like selective in nature and on that basis, these plants are categorized in to metal accumulators and metal excluders (Sinha et al., 2004). The mechanisms behind this have several aspects which make a plant metal accumulator or metal excluder. The basic mechanism which makes a plant phytoremediator is the production of root exudates which enhance the mobility of HMs and nutrients, production of metal chelating agents like phytochelatins (PCs) and metallothionines (MTs), antioxidant compounds like catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), ascorbate peroxidase (ASX), proline, amino acids etc. The soil fertility parameters like pH, EC, presence of nutrients, microbial diversity etc. also affect the contaminant removal ability of the plants. Presence of microbes in the plant growing medium significantly enhances phytoremediation of the contaminants in various ways like by increasing plant biomass, metal bioavailability, metal bioaccumulation in roots (bioaccumulation) and transfer of the accumulated metal in to aerial tissues of the plants (Ma et al., 2011, 2013; Rajkumar et al., 2012; Singh et al., 2014; Baghaie and Aghilizefreei, 2019; Shi et al., 2020).

1.7.1  Plant soil interaction and bioactivation of contaminants For the bioaccumulation of any substance, bioactivation is the first and necessary process. Several toxic substances remain in the soil for longer period without causing any direct adverse effect to the plant. The root exudates released from the roots of the plants are reported not only to enhance the growth and productivity of pants, but also the bioavailability of toxic metals present in soil (Seshadri et al., 2015). The mechanisms of functioning of root exudates in removal of contaminants is done by several ways like altering the rhizospheric soil pH, solubilizing the minerals, chelating, enhancing the microbial number and activities in soil etc. (Yuan-Wen et al., 2003). Kim et al. (2010) observed that the root exudates enhanced the soil pH and dissolved organic carbon which resulted in increased bioavailability of Cd and Zn. They also suggested that among the different factors which govern the metal uptake, root-induced changes in the soil make the phytoremediation process more effective. Root exudates are also reported to be produced during metal stressed conditions (Rengel, 2002). The release of oxalic and malic acids from the root exudates of three plant species Poa annua, Medicago polymorpha and Malva sylvestris in the presence of Cd, Cu and Zn were reported which found to be a vital mechanism to defend the HMs (Montiel-Rozas et al., 2016). Recently, Wu et al. (2019) reported that six organic acids were found to be produced by the plant Leersia hexandra

Phytoremediation 13 Swartz in root exudates in the presence of Cr. It was also observed that the release of these organic exudates significantly enhanced the Cr mobilization. In a study conducted by Lu et al. (2013), it was found that the effect of exogenous application of two organic acids viz. citric acid and tartaric acid on Cd uptake and its translocation in Sedum alfredii was performed. It was observed that the application of both the acids significantly enhanced the metal uptake in the plant.

1.7.2  Contaminant accumulation and translocation into aerial parts The accumulation of contaminants in the plants is the first and most important feature of a phytoremediator plant. The accumulation of contaminants depends on several factors like plant species, level of contamination, soil fertility, microbial diversity in the soil, etc. Baker (1981) and Baker and Walker (1990) classified plants into three categories on the basis of metal accumulation: metal excluder, metal accumulator, and hyperaccumulator plants (Fig. 1.5). 1.7.2.1  Metal excluder plants Metal excluder plants avoid translocating the metals into the aerial parts from the roots, irrespective of the soil metal contamination is higher. The common examples of excluder species are Commelina communis, Oenothera biennis, Agrostis stolonifera, Silene maritime, Populus, Salix, and Pinus radiata (Wei et al., 2005; Maestri et al., 2010). Wei et al.

Fig. 1.5 (A) Metal excluder, (B) metal accumulator, and (C) hyperaccumulator plants.

14  Chapter 1 (2005) found species Oenothera biennis and Commelina communis as Cd-excluders and Taraxacummongolicum as a Zn-excluder among 54 weed species cultivated in the pots. 1.7.2.2  Metal indicator plants Metal indicator plants accumulate metals into the roots and transfer them in their aerial tissues. Although, the level of metal accumulated in tissues of these plants is low but is sufficient to reflect the level of contamination in the environment (Baker and Walker, 1990). These plants are not able to survive in the soil having high level of metal contamination, as they do not bear a strong defense mechanism to overcome the toxic effects exerted by the metals. Metal indicator plants are considered as pollution indicators therefore, are also ecologically significant (Mganga et al., 2011). 1.7.2.3  Metal accumulator plants The plants which actively uptake metals are known as metal accumulator plants. These plants have the efficiency to accumulate the metals up to the levels higher from the soil. The roots of metal accumulator plats absorb the HMs and also transfer them into their shoots. Majority of these plants have tolerance toward the contaminants to survive without exhibiting any adverse effect. For instance, Ricinus communis a species of Euphorbiaceae family has been extensively studied for it metal accumulating potential (Bauddh and Singh, 2012a, b; Bauddh and Singh, 2015a, b; Bauddh et al., 2015, 2016, 2017; He et al., 2020; Palanivel et al., 2020). Among the category of metal accumulator plants, several plant species have been identified for their application in phytoremediation and popularized as hyperaccumulator plants due to their potential to accumulate comparatively higher amount of contaminants in their roots and also transfer them into the aerial parts. These plants have a special characteristic of transfer of metal in to their aerial parts up to a higher level than accumulated in to the roots (Chaney et al., 1997, 2005; Reeves and Baker, 2000; Ellis and Salt, 2003; Reeves, 2003, 2006; PilonSmits, 2005; Sors et al., 2005; Milner and Kochian, 2008). More than 450 plant species have been recognized as metal and metalloids hyperaccumulators especially for Ni, Cu, Zn, Co, Mn, Cd, and As (Reeves and Baker, 2000; Ellis and Salt, 2003; Reeves, 2003, 2006; Sors et al., 2005; Milner and Kochian, 2008). 1.7.2.4  Hyperaccumulator plants The hyperaccumulator plants have specifically designed mechanisms at physiological and biochemical levels to accumulate HM and sustain normal growth without producing severe adverse effects. The secretion of organic acids, protons, enzymes, amino acids in the rhizosphere increases metal bioavailability. Due to the secretion of protons by the roots, rhizosphere is acidified resulting in enhanced dissolution of metal. In solution culture pHdependent proton release and plant growth were observed in Ni-hyperaccumulator plant (Alyssum murale) (Bernal et al., 1994). Some examples of common hyperaccumulators include Sedum plumbizincicola, Pteris vittata, Alyssum serpyllifolium, Thlaspi caerulescens,

Phytoremediation 15 Phytolacca Americana, and Solanum nigrum. Over 500 hyperaccumulator plants have been investigated belonging to the family Asteraceae, Caryophyllaceae, Cunouniceae, Brassicaceae, Cyperaceae, Fabaceae, Flaconrtiaceae, Laminaceae, Poaceae, Euphorbiaceae, etc. (Prasad and De Freitas, 2003; Krämer, 2010). Among these, Brassicaceae family is considered one of the important family having several hyperaccumulator plants.

1.8  Mechanisms behind metal accumulation and their translocation The accumulation of toxic substances from the contaminated medium is the key feature of a phytoremediator plant. Initially HMs get accumulated in the root tissues of the plants. Three roots exudates citric acid, glycine, and maltose were used to assess their impacts on Cd accumulation (Chen et al., 2020). It was found that all three biochemicals enhanced the growth of the plants along with enhanced Cd accumulation in the roots and its translocation into the shoots. Organic acid secretion can mobilize HMs and enhance root absorption. To tolerate Al, plants show either apoplastic or symplastic detoxification mechanism (Ma et al., 2001; Pilon-Smits and Leduc, 2009). Cd organic complex formation was associated with the uptake of 40% of total Cd in the soil and phyto-availability of Cd (Krishnamurti et al., 1997). The metals are complexed with carboxylic acid in the form of citrate for Ni and tartrate or malate for Co (Van der Ent et al., 2018a, 2018b). In T. caerulescens stable Ni-nicotianamine complex is formed in xylem sap (Mari et al., 2006). Co and Ni, bind strongly to roots and are passively absorbed from soil solutions. They enter inside the cell through plasma membrane carriers and may be transported by IRT1 (Iron regulated transporter 1) (Pilon-Smits and Leduc, 2009). The metal Cd is adsorbed by root apoplast and competes with symplastic absorption for accumulation in roots (Redjala et al., 2009). Similarly, plant sp., viz. Stanleya sp. and Astragalus sp. have specialized transporter systems that adapt them to accumulate 1000–1500 ppm (0.1%–1.5%) of Se, even from the low level of soil concentrations. In A. bisulcatus and B. oleracea, specific selenocysteine methyl transferases have been identified that lead to the accumulation of Se (Tamaoki et al., 2008). The transport of Cd in the leaf mesophyll layer is maintained by transporters present in the plasma membrane and tonoplast. It generally affects the Vmax of root without affecting Km (Lasat et al., 1996; Lombi et al., 2001). Mode of Ni uptake in leaf tissue has been explained in A. lesbiacum, where it activates vacuolar H+-ATPase in the presence of Mg/ATP (Ingle and Fricker, 2008).

1.9  Mechanisms of contaminant tolerance in plants Mining and oil drilling sites are key sources of organic and inorganic contaminants such as PAHs and HMs in nearby areas (Sarma et al., 2016). Plants respond to these pollutions quickly and their responses can be categorized as (i) signaling, (ii) detoxification, and (iii) degradation. Various hormones and enzymes including ethylene, brassinosteroids, and

16  Chapter 1 diphosphate kinase have been shown to be involved in response to polycyclic aromatic hydrocarbon exposure and signaling in plants (Weisman et al., 2010; Ahammed et al., 2012; Liu et al., 2015). In plants, the detoxification pathway for PAHs can be categorized as transformation, conjugation, and neutralization/sequestration/export outside the cell. Plants possess various enzymes such as hydrolases, oxidoreductases, carboxylesterases, dioxygenases, cytochromes P450, and peroxidases (POD) for PAH transformation (Campos et al., 2008; Fu et al., 2016; Hernández-Vega et al., 2017). Transformation makes PAHs more reactive which can then conjugate to various endogenous molecules including glutathione, sugars, malonic acid, and amino-acids (Coleman et al., 1997). Conjugation of PAHs with endogenous molecules is catalyzed by various transferases such as glutathione-S-transferases, glycosyltransferases, and malonyl transferases. Conjugation process makes PAHs soluble hydrophilic polar compounds. PAH conjugates are neutralized by the cell wall polymer such as lignin, sequestered via ATP-binding cassette transporters in the vacuoles or exported outside cells (Ishikawa, 1992; Lu et al., 1997). Organic contaminants also induce oxidative stress, through excessive production reactive oxygen species (ROS) accumulation in plant cells, which in turn reduce plant growth and development. Antioxidant enzymes and molecules reduce oxidative stress damages conferred by PAH stress (Shen et al., 2018; Houshani et al., 2019). Carotenoid and SOD were reported as two most active antioxidants for ROS scavenging among 9 main antioxidants SOD, CAT, APX, and glutathione-S-transferase (GST), GSH, ascorbate (AsA), α-tocopherol, polyamines, carotenoid in wheat leaves under phenanthrene stress. Ascorbate-glutathione cycle turns active under higher phenanthrene treatments (Shen et al., 2018). However, Sobhani et al. (2020) reported decreased activity of SOD and POD but increased CAT activity with increase in the concentration of pyrene and phenanthrene compounds in wheat leaves. In comparison to glycophytic Arabidopsis thaliana, halophytic Thellungiell asalsuginea demonstrated enhanced phenanthrene tolerance and recovery from stress. Accumulation of phenanthrene in stomata of T. salsuginea suggested possible volatilization (Shiri et al., 2015). For protection against HMs, plants have developed mechanisms to exclude or detoxify them (Jha et al., 2019; Singh et al., 2019). The first living structure of the cell that encounters HMs is the cell wall. It restricts the movement of HMs into the cytoplasm. Cell wall sequestration of HMs and their limited translocation are considered as HM tolerance mechanisms in plants (Torasa et al., 2019). Plants also secrete a variety of metabolites including low-molecularweight organic-compound in the rhizosphere for detoxification of HM present in soils (Chen et al., 2017; Osmolovskaya et al., 2018). Once metals enter plant cells, they generate signaling molecules such as nitric oxide, ethylene, salicylic acid, jasmonic acid, etc. which contribute to HM tolerance (Popova et al., 2012; Jan and Parray, 2016). Components that cause HM detoxification significantly influence the plant metal tolerance. These components include chelation of metals with different ligands such as PCs, MTs, GSH, chaperons, organic acid, and amino acid and its transportation to above-ground parts and accumulation

Phytoremediation 17 in vacuoles. Thiol groups play a key role in conjugation and detoxification of HMs which need to be sequestered within the vacuole. PCs, MTs, and GSH have a high affinity for HMs due to their thiol groups. PCs are peptides synthesized by enzyme PC synthase. Some of the HMs strongly produce PCs, a sulfur-rich molecule with the capability to bind metals strongly. MTs are low molecular-weight (5–10 kDa) cysteine-rich proteins implicated in homeostasis and tolerance of HM in plants (Cobbett and Goldsbrough, 2002). As MT-metal complexes have high thermodynamic and low kinetic stability, it can tightly bind metals and promptly exchange them with other proteins (Domènech et al., 2007). Organic acids such as oxalate, citrate, malate, etc., bind strongly with HM with their carboxyl groups. They participate in both intracellular and extracellular HM chelation. Secretion of organic acids by plant roots forms an extracellular complex with HM and reduces their bioavailability whereas intracellular chelation by organic acids improves metal tolerance in plants (Osmolovskaya et al., 2018). Sequestration of HMs in vacuoles imparts tolerance to plants. Various families of transporters including HMs ATPases (HMAs), natural resistance-associated macrophage proteins (NRAMPs) Ca2  + exchangers (CAXs), and ATP-binding cassette subfamily C proteins (ABCCs), are associated with sequestration of HMs in vacuoles (Korenkov et al., 2007; Park et al., 2012). Like PAHs, HMs also induce oxidative stress in plants. Enzymatic as well as non-enzymatic antioxidants contribute to HM tolerance by scavenging ROS. Depending on the plant and HM content responses of antioxidant differs. Various studies have reported enhanced ROS formation and considerable enhancement in the activities of SOD, CAT, and APX due to exposure of HMs (Mishra and Sharma, 2019; Sharma et al., 2019). Non-enzymatic components such as ascorbate and GSH also provide tolerance against oxidative stress by protecting plants against HM induced oxidative stress (Asgher et al., 2017; Sharma et al., 2019).

1.10  Molecular mechanisms of phytoremediation of toxicants Various molecular mechanisms enhance the potential of plants to phytoremediate organic and inorganic contaminants, such as PAHs, RDX, TNT, and HMs present in oil drilling and mining sites. Phytoremediation of organic contaminants includes (i) phytoremediation ex planta and (ii) direct phytoremediation (Reichenauer and Germida, 2008). Root exudates containing organic acid, phenolics, proteins, alcohol which are released by plants stimulate the growth and metabolic capabilities of microbes that have the capability of degrading organic contaminants in the rhizosphere (Gao et al., 2010; Sun et al., 2010). Some of these microbes enhance remediation process by breaking down organic pollutants to generate humic substances or volatilizing contaminants such as PAHs (Salt et al., 1998). In plants, there is no known natural transporter for organic contaminants, therefore these contaminants are taken up passively. Uptake of organic contaminants in plants is limited by physicochemical properties, availability, and uptake mechanisms. Physicochemical properties such as hydrophobicity/hydrophilicity, octanol-water partition coefficient, log

18  Chapter 1 Kow, acidity constant. pKa, concentration, and others (Namiki et al., 2018). Compounds that are moderately hydrophobic and have octanol-water partition coefficient ranging from 0.5 to 3 are the most likely contaminants taken up by plants (Ryan et al., 1988). Also, plants differ significantly in their capability to uptake specific contaminants. Evaporation rate is a key player in the uptake of organic compounds and that might be the reason of differential uptake. Natural (rhamnolipids) and artificially produced (SDS, Triton X-100) biosurfactants have been reported to enhance water solubility and bacterial degradation of organic contaminants. Mixed surfactants (sodium dodecylbenzene sulfonate and Tween 80 in 1:1, 1:2, and 2:1 ratio) could also enhance phytoremediation of PAHs in soil. It enhanced the quantity of PAHs degrading bacteria and degradation related genes (Lu et al., 2019). Cyclodextrins also solubilize organic contaminants (Shirin and Buncel, 2005). Partitioning of various contaminants vary significantly between root and aboveground parts. After uptake, organic contaminants may (i) get translocated to other plant part and get volatilized (ii) get partially and fully degraded (iii) get transformed to less toxic compounds (iv) bind to plant tissue such as insoluble lignin and remain non-available (v) get sequestered in vacuoles. Lipid bilayer of the plasma membrane and hemicellulose of cell wall bind hydrophobic organic contaminants (Pilon-Smits, 2005). Various chemical reactions including oxidation, reduction, and hydrolysis can modify organic contaminants which can then conjugate with organic acids, sugars, and GSH. Conjugation enhances solubility and movement of organic contaminants into vacuoles, where they can be further metabolized to CO2 and water (Campos et al., 2008). GST enzyme catalyzes the transfer of GSH to organic contaminants which results in detoxification of organic contaminants (Schröder et al., 2008). ATP-dependent membrane pumps actively transport glutathione S-conjugates to the vacuole/ apoplast. In hyperaccumulators, cytochrome P450 participates in degradation and hence phytoremediation of organic pollutants (Rostami and Azhdarpoor, 2019). Plants can detoxify RDX and TNT up to a limited extent. Direct conjugation of the TNT molecule with glutathione by GSTs has been shown (Gunning et al., 2014). Expression of GST (DmGSTE6) from Drosophila melanogaster in Arabidopsis improved its TNT phytoremediation potential (Tzafestas et al., 2017). The TNT transformation is also done by the enzyme oxophytodienoate reductases which is then subsequently conjugated by the enzyme uridine diphosphate glycosyltransferases (GandiaHerrero et al., 2008; Beynon et al., 2009). Transgenic Agrostis stolonifera and Panicum virgatum expressing xplB (flavodoxin reductase) and xplA gene (cytochrome P450 activity) also showed better removal of RDX (Zhang et al., 2017). Arabidopsis plants expressing XplA and partnering XplB from Rhodococcusrhodochrous strain 11Y and nfsI from Enterobacter cloacae which encodes a nitroreductase showed enhanced TNT detoxification and RDX degradation (Rylott et al., 2011). Recently, a putative flavonol synthase has been shown to be involved in detoxification of PAHs in Arabidopsis thaliana (Hernández-Vega et al.,

Phytoremediation 19 2017). Different plant growth regulators such as cytokinins, gibberellins, salicylic acid, and auxins also increase the phytoremediation efficiency of organic contaminants (Rostami and Azhdarpoor, 2019). They enhance the plant biomass and reduces the harmful effects of organic contaminants in the plant. Like organic contaminants, phytoremediation of HMs also includes several steps, such as: (a) secretion of various compounds in rhizosphere to augment the mobility of contaminants, (b) transport of contaminants through root cell plasma membrane, (c) translocation through xylem, (d) detoxification of contaminant, and (e) sequestration of contaminants. Among HMs, some like Cd and Zn are more available and mobile for uptake in plants compared to others which are comparatively immobile like Pb (Lasat, 1999). Soil pH and presence of chelating compounds like EDTA can enhance metal mobility and hence uptake of metals. Concentration of metals, metal interaction, temperature, organic matter, nutrients, microbial consortium, etc., also play a role to influence the mobility of metal ions in soil (Rieuwerts et al., 1998; Luo et al., 2016; Cui et al., 2019). The enzyme secretion by microorganisms present in the plant’s rhizosphere makes metal ions available for absorption by roots (Burns and Dick, 2002). Several processes are used by plants to increase the availability of metal ions e.g. acidification of the rhizosphere, secretion of organic acids such as malate, citrate, phytosiderophores which enable the solubilization and chelation of soil-bound metals (Kinnersley, 1993). The changes in composition and content of root exudates that facilitate phytoremediation of HM contaminated soils take place upon exposure to metals (Javed et al., 2017; Ping et al., 2017). Hou et al. (2015) observed more secretion of organic acids, including citric, succinic, and glutaric acid under lead stress. These organic acids have the capability to increase uranium accumulation in plants by desorbing uranium in soil colloid and enhancing the content of free-moving HMs. Metallic contaminants enter roots through apoplastic/symplastic pathway. Cell walls have a comparatively high exchange capacity for cations (Raskin et al., 1997). Thus, as many metals are insoluble and incapable of moving in the vascular system themselves, they are immobilized in apoplastic and symplastic compartments after forming carbonate, sulfate, or phosphate precipitates (Raskin et al., 1997; Garbisu and Alkorta, 2001). Metal chelates can follow apoplastic movement. Metal hyperaccumulator plants translocate a very high concentration of metal ions into the shoot via symplastic movement through the xylem. Through root symplasm, HMs enter xylem stream (Tester and Leigh, 2001). After uptake, metallic contaminants translocation takes place through xylem vessel by xylem loading. In shoot, unloading of metallic contaminants takes place in sap of the xylem. Metal entry from root tissue to xylem is primarily regulated by three activities: metal ion sequestration in root cells, symplastic transport in stele, and discharge in xylem (Ghosh and Singh, 2005; Saxena and Misra, 2010; Cui et al., 2019; Hu et al., 2019). The metallic contaminants sequestration begins when it is taken up in root cells where they bind to cell

20  Chapter 1 wall components such as pectin and suberin (Baxter et al., 2009; Parrotta et al., 2015). Many low-molecular-weight organic compounds, e.g., GSH, non-proteinogenic amino acids, and organic acids having metal chelating properties are used by plants to detoxify, sequester, or transport metals (Krämer, 2003; Osmolovskaya et al., 2018; Dubey et al., 2018). They can be manipulated to improve phytoremediation process. Nicotianamine plays an important role in detoxification of metals and has been proposed as an important tool for utilization in phytoremediation. Overexpression of HvNAS1 gene from Hordeum vulgare in Arabidopsis plants led to increased accumulation of Ni. Metals also form complex with thiol chelators, e.g., PCs, GSH, MTs. These metal chlelators play a key role in phytoremediation of HMs such as Zn, As, Cu, and Cd (Srivastava, 2016). Tobacco and Arabidopsis plants overexpressing MnPCS1 and MnPCS2 from Morusnotabilis exhibited increased Cd and Zn phytoremediation (Fan et al., 2018). Cu exists as thiol-S bound Cu(I) complex in root xylem (Cui et al., 2019). Hence, the reduction of Cu (II) to Cu (I) in rice roots is considered as an adaptive Cu stress tolerance mechanism with phytoremediation implications (Cui et al., 2019). Metal chelator complexes are transferred from cytosol to vacuoles (Song et al., 2014). Vacuolar sequestration of HM contaminants is an important molecular mechanism for the purpose of phytoremediation (Zhang et al., 2018; Rai et al., 2020; Tan et al., 2019). Metal sequestration in roots restrict its translocation to aerial parts. Vacuoles contain many transport proteins such as ATP-binding cassette (ABC) family (AtSuc4); vacuolar sugar transporters; vacuole iron transporter (VIT) H+-ATPase; Na+/H+ antiporter; Ca2  +/H+ antiporters; multidrug and toxic compound extrusion (MATE) for the sequestration of HM contaminants (Zhang et al., 2018; Tan et al., 2019). In transgenic studies, ABC genes were found localized in tonoplast and improved metal sequestration in lumen of vacuoles (Yazaki et al., 2006; Song et al., 2014). Metal tolerance/transport protein (MTP) which is encoded by cation diffusion facilitator (CDF) family participates in excluding excessive ions from the cytoplasm. Overexpression of CDF genes enhanced thiol concentration and metal chelation and led to efficient vacuolar sequestration and hyperaccumulation of metals in plants. Tobacco plant overexpressing OsMTP1 from indica rice caused Cd hyperaccumulation and increased arsenic accumulation and tolerance upon exogenous Cd and As treatments suggesting wide substrate specificity of this transporter (Das et al., 2016). The HMW compounds get dissociated in vacuoles owing to acidic pH and then chelated with organic acids (e.g., amino acids, oxalate, citrate, and malate) (Choppala et al., 2014; Luo et al., 2016; Rai et al., 2020). In addition to vacuoles, Golgi apparatus has been associated with exocytosis of metals, facilitating phytoremediation (Shi et al., 2019; Rai et al., 2020). Metal sequestration inside compartments of cells can be a mechanism to detoxify and hence protect the important enzymes and metabolites actively associated with metabolic machinery. Furthermore, the role of antioxidants in scavenging excess ROS due to HMs is a key strategy for metal tolerance and hence important for successful HM phytoremediation (Ali et al., 2003; Goswami and Das, 2016).

Phytoremediation 21

1.11  Phytomining a win-win aspect of phytoremediation Conservation of natural resources and protection of the environment, poor quality ore exploitation, and secondary metal resource recovery has become critical these days. Phytomining is a plant-based mining technology in which accumulator or hyperaccumulator plants are used to accumulate soil metals into aerial parts of the plant e.g. shoots, where they are treated as “bio-ore” for the recovery of metals (Robinson et al., 1997; Anderson et al., 1999; Van der Ent et al., 2018a, 2018b; Chen et al., 2020). Through this technology, the metals can be recovered from sub- or low-grade ore bodies, metal-contaminated soils, mineralized (ultramafic) soils, mine tailings. Similar to phytomining, agro-mining harvests bio-ore from the “crops” that grow on the degraded lands (Jiang et al., 2015). These two technologies have different sources of bio-ore raw materials. In the phytomining accumulators or hyperaccumulators plants and agro-mining high biomass yielding crops are used to harvest the metals. Agro-mining can be considered as a variant of phytomining (Van Der Ent et al., 2015); in the present chapter, it is discussed from the perspective of phytomining. Owing to the higher rate of depletion of metal and mineral resources and the increase in global demand for metals, phytomining has gained much global attention in recent years, because phytomining can harvest high-grade, sulfide-free or low-sulfide bio-ore, it has potential applications in the mineral industry as an environmentally sound and sustainable mining technology (Maluckov, 2015; Svanbäck et al., 2015; Rosenkranz et al., 2019). Sometimes when elements are phyto-extracted to remediate soils, the recovered biomass may have low economic value (like Cd, As, etc.) and disposal of the biomass would be expensive, on the other hand, few elements are highly valuable (like Ni, Co, Au) in phytomining. For phytomining purposes, plant species should be high-biomass yielding and hyperaccumulator (Chaney et al., 2018). Furthermore, for increasing the success of phytomining proper understanding of metal hyperaccumulation physiology is required (Verbruggen et al., 2009). In general, whenever a plant is exposed to metals, four probable interactions are possible: (a) Some metals that share properties with required nutrient cations, may compete for root absorption, for example, As and Cd show competition with P and Zn, (b) Some metals interact with sulfhydryl group (-SH) of proteins, thus disrupting their structure and function and making them inactive, (c) Some metals displace essential cations from their active (specific) binding sites, thus affecting their functions and. (d) Metals generate ROS, which damage the macromolecules (Sharma and Dietz, 2009; Dalcorso et al., 2013) For phytomining selection of appropriate hyper accumulating plants, and knowledge regarding bioavailability of metal species in the substrate and extent of toxicity for the plants is a prerequisite (Kramer, 2018). For example, the plant species and method using for phytomining of platinum group metals involves the plants growing on PGM-rich substrates

22  Chapter 1

Fig. 1.6 Characteristics of plants ideal for phytomining.

that are efficient of selectively incorporating the metals into their cellular structures (Sheoran et al., 2009). In another study, Parker et al., (2014) reported the first use of living plants to recover palladium (Pd) followed by production of catalytically active Pd-nanoparticles with significant catalytic activity across a range of coupling reactions that produced higher yield than commercial Pd catalyst was reported. Fig. 1.6 shows the characteristics of plants ideal for phytomining.

1.12 Conclusion Several sources, mining, in particular, entail the release of HMs into the environment (both soil and water ecosystems). Removal of contaminants from the soil, water, sediments, and even air using green plants is highly efficient technology. Different aspects of phytoremediation can be applied depending on the types and levels of contamination. Several plants have been identified as hyperaccumulators, which can extract the contaminants significantly in a larger amount. Initially phytoremediation was invented to remove the inorganic contaminants especially HMs, but now it is applying for the degradation of organic contaminants as well as restoration of abiotic stressed soils like salinity and drought-affected land, mining spoiled sites, and other wasteland and marginalized land. Cultivation of phytoremediator value-added crops on the contaminated sites makes this technology more attractive. Phytomining is another pivotal aspect of phytoremediation through which recovery of essential minerals from the mining sites may be done very efficiently. Phytoremediation enhances the aesthetic and recreational values to the society. Phytoremediation also helps in carbon sequestration that is helpful in the mitigation of global climate change.

Phytoremediation 23

Acknowledgments K.B. is thankful to Science and Engineering Research Board (SERB), New Delhi, India for the award of research grant (EEQ/2017/000476. P.S. acknowledges DST-SERB project no. ECR/2016/000888 and UGC-Start-up Grant No. F.4-5(107-FRP)/2014(BSR) for financial support). R.S. acknowledges DBT-BioCARe project no. BT/ PR30922/BIC/101/1184/2018 funded by DBT, India for financial support.

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32  Chapter 1 Weisman, D., Alkio, M., Colón-Carmona, A., 2010. Transcriptional responses to polycyclic aromatic hydrocarboninduced stress in Arabidopsis thaliana reveal the involvement of hormone and defense signaling pathways. BMC Plant Biol. 10, 59. https://doi.org/10.1186/1471-2229-10-59. Wu, C., Liu, J., Liang, Y., Jiang, Y., Zhang, X., 2019. The low molecular weight organic acids in root exudates of Leersia hexandra Swartz and its role in mobilization of insoluble chromium. IOP Conf. Ser.: Mater. Sci. Eng. 484, 012009. Yazaki, K., Yamanaka, N., Masuno, T., Konagai, S., Kaneko, S., Ueda, K., Sato, F., 2006. Heterologous expression of a mammalian ABC transporter in plant and its application to phytoremediation. Plant Mol. Biol. 61, 491–503. Yuan-Wen, K., Da-Zhi, W., Chuan-Wen, Z., Guo-Yi, Z., 2003. Root exudates and their roles in phytoremediation. Acta Phytoecol. Sin. 27 (5), 709–717. Zazouli, M.A., Mahdavi, Y., Bazrafshan, E., et al., 2014. Phytodegradation potential of bisphenol A from aqueous solution by Azolla Filiculoides. J. Environ. Health Sci. Eng. 12, 66. https://doi.org/10.1186/2052-336X-12-66. Zhang, L., Routsong, R., Nguyen, Q., Rylott, E.L., Bruce, N.C., Strand, S.E., 2017. Expression in grasses of multiple transgenes for degradation of munitions compounds on live-fire training ranges. Plant Biotechnol. J. 15, 624–633. Zhang, J., Martinoia, E., Lee, Y., 2018. Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development. Plant Cell Physiol. 59, 1317–1325.

CHAPTE R 2

Phytoremediation of abandoned mining areas for land restoration: Approaches and technology Lakshmi Pathak and Kavita Shah Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, India

2.1 Background Numerous natural as well as anthropogenic activities have tremendously changed the quality of soil and have increased the level of heavy metals therein. Majority of anthropogenic sources include the usage of pesticides, petrochemical, textile, leather, construction, manufacturing, food processing, mining industries, and coal combustion (Bhargava et al., 2012; Mahar et al., 2016; Zhao et al., 2010). Mining and coal-producing activities from surface mines, ore, and fly ash disposal have led to a changed landscape. These activities resulted in poor air, soil, and water quality, loss of flora-fauna, and negative impact on human health (Gajić et al., 2018a,b; Mukhopadhyay and Maiti, 2010). Mine waste and fly ash contain fine particles, metal(loid)s and persistent organic pollutants (POPs) that if released inappropriately would lead to air, water, and soil pollution (Jala and Goyal, 2006). Further dispersal of fine particles caused by wind affects human health and causes eye, skin, nose, and throat irritation along with respiratory system infections as asthma, bronchitis, and lung cancers (USEPA, 2004). The treatment, detoxification, and restoration of contaminated mining areas are one of the major environmental issues worldwide. Mining dust of metalliferous ores or leachate in groundwater and soil is often a challenge for removal. Heavy metals are generally found in environment naturally, but their nonselective and unmethodical use has changed biogeochemical cycle making them enter into food chain which is injurious for animals, plants, human and environmental health (Shah and Dubey, 2000). Few heavy metals are endocrine disruptors, teratogenic, carcinogenic, and mutagenic while few of them cause behavioral and neurological changes, particularly in children. This draws due attention toward remediation of heavy-metal pollution in the environment. Physicochemical techniques used for remediation of multimetal contaminated sites require high cost, are labor intensive, Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00008-X © 2021 Elsevier Inc. All rights reserved.

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34  Chapter 2 and are preferred for decontamination of small land area. However, these methods are not applicable to agricultural areas as they may hamper soil fertility during excavation or chemical treatment. Phytoremediation is referred as “green remediation” which encourages the conservation of natural resources and minimization of environmental impacts (RTI, 2007). Interest in decontamination of wastelands has increased globally as demands for food, feed, and fuel continue to rise at unprecedented rates. The biomass energy policy of India also favors the use of wastelands for growing short rotation woody trees, nonedible plants and grasses as well as bioenergy crops for decontamination of soil (Pathak and Shah, 2019) to avoid fuel vs food security dilemma. These plant biomasses serve as feedstock for bioenergy generation; however, decomposition of lignocellulosic component of plants needs biochemical or enzymatic or thermochemical treatment prior to use (Pathak and Shah, 2017). Phytoremediation process is widely recognized as economically viable and environmentally sustainable alternative when compared with conventional remediation technologies used for removal and treatment of indiscriminate hazardous waste discharged in soil and water largely by extracting, stabilizing or modifying the waste into less toxic forms (Shah, 2011; Susarla et al., 2002; USEPA, 2008; Wang et al., 2007). Constructed wetlands, floating-plant systems, and reed beds systems have been used commonly for different wastewater treatments for several years. Deploying green plants to extract and degrade heavy metals is an ecofriendly substitute to combat the negative effects of physicochemical remediation methods (Meagher, 2000; Raskin et al., 1997). The process utilizes solar-driven remediation strategy which is comparatively cheaper than other technologies already in use (Chehregani and Malayeri, 2007; Clemens, 2001; Kawahigashi, 2009; Lone et al., 2008; Odjegba and Fasidi, 2007; Sarma, 2011; Singh and Prasad, 2011; Vithanage et al., 2012). Therefore, coupling of phytoremediation process with plantation of bioenergy rich plants is advantageous and unique owing to selective uptake capabilities of different plant root systems for different heavy metals from the environment and their detoxification is also accomplished by various mechanisms limiting their translocation and enhancing their degradation, bioaccumulation, and storage. Global hyperaccumulators include more than 400 plant species (Raskin and Ensley, 2000) of which the majority are discovered for hyperaccumulation of Ni, whereas species accumulating As, Cd, Co, Cu, Pb, and Zn are relatively low (Bhargava et al., 2012). Family Brassicaceae is rich in hyperaccumulators (Alyssum, Brassica, and Thlaspi). Viola calaminaria is reported to accumulate high concentration of heavy metals in their aboveground part under natural conditions (Raskin and Ensley, 2000; Shah and Nongkynrih, 2007). The phytoremediation processes are able to treat multimetal contaminated site and avoid risk of contamination which is spread during excavation and transport of polluted soil (Saxena et al., 2019). Plants uptake the heavy metals and other pollutants without affecting top soil, thereby conserving its utility and fertility. However, phytotechnology has limitations as it is dependent upon abiotic (e.g., climate, altitude, temperature) and biotic conditions (e.g., plant growth conditions); access to agricultural equipments and knowledge for large-scale operations and level of tolerance of plant species for the pollutants (Mudhoo et al., 2010).

Phytoremediation of abandoned mining areas for land restoration  35 Selection of hyperaccumulator plants from a wide variety and groups of plants is a major step for achieving high bioaccumulation and improved translocation factor of metal(s) from soil to plant. If energy harvesting and elemental recovery is a primary concern then other factors such as biomass yield, tolerance limit, and growth rate of plants are important criteria of consideration. To meet the demand for energy supply the harvested energy crop biomass can be used as renewable energy sources (RES) (Mleczek et al., 2010; Rowe et al., 2009). Ecorestoration and phytoremediation of mining sites often witness unfavorable conditions. The understanding and criteria for selection of indigenous plant species for establishing self-sustaining vegetation cover for eco-restoration of contaminated sites is therefore essential. The phytoremediation technologies available or in use for decontamination of mining areas are discussed.

2.2  Physicochemical characteristics of mine soils Mining areas mostly have poor soil structure, coarse texture with more sand fractions and less clay content. Mine soil has low content of essential nutrients, e.g., nitrogen, phosphorus as compared to naturally occurring soil (Mukhopadhyay et al., 2013). Soil of mining areas show a large variation in pH ranging from acidic to slightly alkaline (2.5–7.5) and electrical conductivity ranging between 6.4 and 18 dS/m (Bes et al., 2014; Conesa et al., 2006; Fernández et al., 2017; Gomez-Ros et al., 2013) (Table 2.1). The availability of organic carbon and total nitrogen range between 0.5%–33.3% and 0.04%–1.2%, whereas potassium and phosphorous fall within the range 42.3–129.0 g kg−   1 and 0.9–74.3 mg kg−   1, respectively, suggesting large variations in soils of mining areas which in turn depends upon climatic conditions and level of contamination (Bes et al., 2014; Conesa et al., 2006; Parraga-Aguado et al., 2013; Ranđelović et al., 2016; Santos et al., 2016) (Table 2.1). The mine soil contains Table 2.1: Plant species growing on mine waste with high potential for phytoextraction and phytostabilization. Plants Cistus ladanifer Ricinus communis Holcus lanatus Epilobium dodonaei Helichrysum decumbens Euphorbia pithyusa Cynodon dactylon Acacia retinodes

Heavy metals Phytoextractor

References

Al, Ag, Ba, Bi, Sr, Sb Cd, Cu, Mn, Pb, Zn As, Hg As, Cd, Cu, Pb, Zn Al, Ag, Ba, Bi, Sr, Sb Cu, Pb, Zn Pb, Zn As, Cd, Cu, Pb, Zn

Santos et al. (2016) Olivares et al. (2013) Fernández et al. (2017) Ranđelović et al. (2016) Conesa et al. (2006) Jimenez et al. (2011) Madejon et al. (2002) Gomez-Ros et al. (2013)

Phytostabilizer Coincya monensis Polygonum aviculare Dittrichia viscosa

Al, Ag, Ba, Bi, Sr, Sb Cd, Cu, Mn, Pb, Zn As, Hg

Santos et al. (2016) Olivares et al. (2013) Fernández et al. (2017)

36  Chapter 2 high concentrations of not one but several metals (As, Cd, Cu, Fe, Hg, Mn, Ni, Pb, Zn) that exceed the maximum permissible limit standards of agricultural/commercial/industrial/ residential use guidelines (Bes et al., 2014; Gomez-Ros et al., 2013; Parraga-Aguado et al., 2013; Ranđelović et al., 2016; Santos et al., 2016).

2.3  Remediation of abandoned mining areas The byproducts of coal production and mining activities get deposited in open-air tailing ponds and are generally referred as mine tailings (Babel et al., 2016). These tailings consist of a mixture of fine particles, sand, heavy metals, and water (Santibañez et al., 2012). Mine tailing discharges lead to degradation of land and deterioration of air as well as water quality, negatively affecting flora-fauna, and human beings (Jala and Goyal, 2006; Mukhopadhyay et al., 2013; Gajić et al., 2018a,b). The nondegradable heavy metals or organic pollutants discharged in large amounts bear a negative impact on the ecosystem (Dary et al., 2010). High heavy-metal concentrations in soil are known to cause leaf chlorosis, suppress plant root growth, and result in low biomass production (Jadia and Fulekar, 2009; Singh et al., 2019). Except for Antarctica, the mining activities occur in all the continents of the world (Munshower, 2018). Mine tailings discharge is reported to have exceeded 10 billion tons globally (Adiansyah et al., 2015) and has led to allergies, eyes, nose, throat, and respiratory infections and diseases such as anemia, asthma, bronchitis, cancer, etc. (USEPA, 2008). Although the soils can be remediated of contamination by various physical and chemical treatments such as capping, excavation and chemical stabilization ranging from approximately 130,000 to 1,600,000 US$ ha−   1(Berti and Cunningham, 2000), but they are very expensive and likely to add the risk of secondary contamination (Gomez-Ros et al., 2013). Major characteristics of mine tailings include poor physical structure primarily composed of silt/sand particles, a wide range of acidity (pH 2–9), presence of heavy metals and lack of nutrients (Mendez et al., 2007; Rosario et al., 2007; Ye et al., 2002). Primarily toxicity in mine tailings is driven by low pH which increases the bioavailability of metals in the soil (Stevenson and Cole, 1999). Fig. 2.1 enlists various sources of heavy-metal pollution in soil. Heavy metals are toxic elements that occur in earth crust naturally but their unregulated use and release into the environment pose several health hazards and deteriorate soil, air, and vegetation quality. Phytoremediation emerges as a suitable alternative for decontamination of large mine tailing areas with negligible risk of secondary contamination. The most common heavy metals in contaminated soils are As, Cd, Cr, Cu, Hg, Pb, Zn, etc. Natural processes also contribute toward heavy-metal(loid) contamination of soils resulting from weathering of underlying bedrock (Shakoor et al., 2015). Anthropogenic sources of heavy-metal pollution include refining or mining of ores, waste disposal from fertilizer and pesticide industries, paper industries, tanneries, vehicular exhaust, sewage sludge, etc. (Niazi et al., 2015; Shahid et al., 2015). Consumption of contaminated wood with heavy metals is considered to be one of the major pathways to human exposure (Mombo et al., 2015;

Phytoremediation of abandoned mining areas for land restoration  37

Fig. 2.1 Sources of heavy-metal pollution.

Xiong et al., 2016). Therefore, in situ methods such as phytoremediation are preferred which are more economical and less environmentally disruptive. Fig. 2.2 shows various types of remediation techniques used for soil decontamination including in situ or ex situ treatments through physical, chemical, or biological method. Fig. 2.3 illustrates the types of remediation processes occurring in plants.

Fig. 2.2 Various types of remediation techniques used for decontamination of soil.

38  Chapter 2

Phytodegradation Phytovolatilization

Accumulation from roots to shoots

Phytoextraction

Movement from root to shoot

Harvested biomass used for metal recovery

Phytoextraction Phytodegradation Phytostabilization

Fig. 2.3 Types of remediation processes occurring in plants.

2.3.1  Physical remediation 2.3.1.1  Soil replacement It includes excavation and off-site disposal of contaminated soil along with importing new soil on the contaminated land. This method is employed to minimize the concentration of heavy metal(loid)s in soil and improve its functionality (Yao et al., 2012). The off-site disposed soil may be treated for removing heavy metals or dumped directly at other places. The cost of labor, excavation area, and transportation distance lies between 270 and 460 USD per ton of soil replaced (Khalid et al., 2017) during the process; however, the technique is not applicable for agricultural sites as it involves risk of loss in soil fertility. 2.3.1.2  Soil isolation Soil isolation involves installation of barriers to prevent off-site movement of heavy metals and is often advantageous as it helps in the confinement of metals within the specified area

Phytoremediation of abandoned mining areas for land restoration  39 (Zheng and Wang, 2002; Zhu et al., 2012). These installed barriers are limited to 30 ft. depth of soil and are mostly made of low-permeable material such as clay sheet piles, grout curtains, and slurry walls (Rumer and Ryan, 1995). 2.3.1.3  Soil vitrification High-temperature soil treatment reduces the mobility of heavy metals at the contaminated sites and formation of vitreous material (Mallampati et al., 2015) for, e.g., heavy-metal mercury (Hg) volatilizes under high temperature. Navarro et al. (2013) carried out hightemperature treatment of Ag-Pb waste from Spain mines using solar cells. Additionally the process led to immobilization of Cu, Fe, Mn, Ni, and Zn at 105°C. The in situ method has low cost and less energy consumption over ex situ method of excavation, pretreatment, melting, and casting (Dellisanti et al., 2016). Compared with phytoremediation costs of 25–100 USD per ton of soil the vitrification is more cost intensive and involves 300–500 USD per ton of soil (USEPA, 2004). 2.3.1.4  Electrokinetic remediation Electrokinetic remediation of soil involves separating heavy metals via electrophoresis or electro-migration from the contaminated soil (Yao et al., 2012). Nearly 60% of total Hg has been remediated from 400 kg of soil within 3 months through this process (Rosestolato et al., 2015). The method is cost-effective, easy to install and operate, and moreover does not disturb the soil quality; however, pH fluctuation becomes the limiting factor (Page and Page, 2002). The coupled electrokinetic phytoremediation process increased the solubility of As, Cs, and Pb, while lowering the soil pH around 1.5 times which further increased the overall solubility, bioaccessbility, and bioavailability of metals in the soil (Mao et al., 2016).

2.3.2  Chemical methods 2.3.2.1 Immobilization The technique of immobilization is used to increase the availability of heavy metals in aqueous solutions. The process involves the addition of immobilizing agents that decrease mobility of metals, their bioavailability, and accessibility from contaminated soil. Immobilization of metals can be carried out by adsorption, complexation, and precipitation. Soil amendments commonly used are cement, zeolites, clay, mineral phosphates, microbes, etc. (Sun et al., 2016). The potential of economical industrial residues such as farmyard manure (FYM), red mud, termitaria (Anoduadi et al., 2009), industrial eggshell (Soares et al., 2015) is frequently used for immobilization of Cr, Fe, Ni, Mn, and Pb, while di-ammonium phosphate (DAP) was found to be effective in stabilizing Cu, Zn, and Cd in soil. Addition of biochars has significantly reduced mobility and availability of heavy metals (Al-Wabel et al., 2015; Puga et al., 2015).

40  Chapter 2 2.3.2.2 Encapsulation Encapsulation of toxic metal solutions in manageable solid blocks is an alternative method to limit mobility of metals for their proper disposal (Ucaroglu and Talinli, 2012). Encapsulation effectively prevents leaching of organic materials in the soil (He and Chen, 2014). Process of encapsulation requires mixing of the contaminated soils with concrete, common lime, asphalt or any other product immobilizes and contains the contaminated soil from entering the surroundings. In this process, cement is commonly used due to its cost-effective, versatile, and easily available nature (Pandey et al., 2012). Agar, alginate, chitosan, polyvinyl alcohol, polyacrylamide, and polyurethane are also majorly used as immobilization agents. 2.3.2.3  Soil washing Soil washing is a proven rapid, highly efficient and cost-effective method for the removal of heavy metals from contaminated soil using various extractants without any long-term liability (Guo et al., 2016; Park and Son, 2017). Organic acids, surfactants, chelating agents (EDTA), humic substances, and cyclodextrins are commonly used extractants (Kulikowska et al., 2015; Shahid et al., 2014). Removal of lead (Pb) from contaminated soil using 10 mmol kg−   1 EDTA would cost approximately 30,000 USD ha−   1 to attain Pb level of 10 g/kg dry weight (Chaney et al., 2002). Similar field remediation study carried out by Shahid et al. (Shahid et al., 2012) suggested that this reduces the cost of remediation if low EDTA concentration of 2.5–10 mM is used in fields.

2.4  Native plants revegetated and surveyed in mining areas Indigenous plants growing on mine tailings show stress tolerance and perform extraction, stabilization, and degradation of heavy metals naturally. The selection of appropriate plants for revegetation and remediation of contaminated area depends on the following characteristics (i)–(viii) (Ali et al., 2013; Bhargava et al., 2012; Mahar et al., 2016)

(i) (ii) (iii) (iv) (v) (vi)

Short plant growth cycle and high biomass production Widespread roots and stress-tolerant growth May grow in other than native area Higher accumulation and translocation rate of heavy metals in selected plant species Heavy metals toxicity tolerant Adaptable to agro-climatic conditions (drought, humidity, salinity, temperature, nutrient and water stress) (vii) Easy biomass harvesting and resistance against pest attack (viii) Herbivores are repulsive to restrict entry in food chain Plant species (e.g., Agrostis stolonifera, Calamagrostis epigejos, Cerastium arvense, Polygonum aviculare, and Tussilago farfara) have the capability to grow in flotation Cu ore

Phytoremediation of abandoned mining areas for land restoration  41 mine tailings in Poland (Kasowska et al., 2018). Several plant species (Agrostis capillaries, Betula pendula, Chenopodium botrys, Equisetum palustre, Rumex acetosella, Vicia hirsute, Xanthium italicum, Vulpia myuros, Populus tremula, Populus alba, and Populus nigra) were observed to grow in Timok River floodplain that are partially damaged by slurry sulphidic waste from Cu mine in Serbia (Nikolic and Pavlovic, 2018). Indigenous varieties like A. stolonifera, C. epigejos, Cirsium eriophorum, Daucus carota, Epilobium dodonaei, Robinia pseudoacacia, and Rumex crispus were reported to grow on nonreclaimed and reclaimed Cu mine sites in Bor in Serbia (Ranđelović et al., 2016). Few other region specific plant species such as Cistus salviifolius, Dittrichia viscosa, and Euphorbia pithyusa were found to grow in mining sites in Sardinia (Jimenez et al., 2011). Abandoned Pb mine area in Portugal revegetated with Digitalis purpurea, Mentha suaveolens, and Ruscus ulmifolius (Pratas et al., 2013). In addition, Lygeum spartum, Helichrysum decumbens, Tamarix, Zygophyllum fabago, Pinus halepensis, Tetraclinis articulata were observed to grow around Cartagena-La Union mining district, Spain (Conesa et al., 2006; Parraga-Aguado et al., 2014). Plant species such as Agrostis durieui, Coincya monensis, Dactylis glomerata, Festuca rubra, Holcus lanatus, Genista legionensis, Lotus corniculatus were more prevalent in Pb-Zn and Hg-As mining waste in Spain (Fernández et al., 2017). Ricinus communis abundantly observed in Mexico mine tailings (Olivares et al., 2013). In abandoned mine tailings of Sonora, Mexico Amaranthus watsonii, Acacia farnesiana, Bromus catharticus, Baccharis sarothroides, Brickellia coulteri, Solanum lumholtyianum, Gnaphalium leucocephalum, Prosopis velutina, etc. has been identified (Santos et al., 2017). Artemisia annua, Medicago sativa, Festuca elata, Ipomea purpurea, Grewia biloba, Salsola collina, Sonchus oleraceus, Vitex negundo, and Ziziphus jujube were found to grow on soil rock mixture in abandoned mines of Beijing in China (Zhang et al., 2014). Similarly, Cynodon dactylon, Digitaria sanguinalis, Erigeron canadensis, Melastoma dodecandrum, Pteris multifida colonized Mn mine areas of China (Li et al., 2007). Paspalum fasciculatum showed phytoextraction capacity for Pb with high concentrations of metals in tissues and phytostabilization effect for Cd in affected areas near gold mining sites. Plant species is reported to increase Ph and organic matter in the soil rhizosphere (Salas-Moreno and Marrugo-Negrete, 2020).

2.5  Phytoremediation of abandoned mining areas Phytoremediation is recognized as an economical, holistic, and eco-friendly approach to reduce, remove, extract, and degrade pollutants from soil (Padmavathiamma and Li, 2007; Prasad, 2003). Different phytoremediation strategies are phytoextraction, phytodegradation, phytostabilization, and phytovolatilization (Alkorta et al., 2004). Two largely practiced phytoremediation techniques in treatment of mine tailings are phytoextraction and phytostabilization.

42  Chapter 2

2.5.1  Phytoextraction in mine areas Phytoextraction is solar-driven technique for moderately polluted sites and is based upon the uptake capability of the plant roots and accumulation and translocation of heavy metals in aboveground harvestable shoot (Rascio and Navari-Izzo, 2011; Sabir et al., 2015). Plant species that have efficiency to accumulate >   100 mg kg−   1 Cd and Se; >   1000 mg kg−   1 As, Cu, Ni, Pb, and >   10,000 mg kg−   1 Mn, Zn concentration on dry weight basis without any visible toxicity symptoms are known as hyperaccumulator plants (Ali et al., 2013; Mahar et al., 2016). Brassica juncea is reported for Pb remediation in soil when Pb level is greater than 1500 mg kg−   1 (Blaylock et al., 1997). The multiple metal hyperaccumulator plant species known is Thlaspi caerulescens for Cd, Ni, Pb, and Zn (Ali et al., 2013), Thlaspi ochroleucum and Thlaspi goesingense for Ni and Zn; Thlaspi rotundifolium for Ni, Pb, and Zn (Keller and Hammer, 2004; Vogel-Mikuš et al., 2006). Few species of Brassicacea and Leguminosae are reported to accumulate multiple metals at high concentrations (Kotrba et al., 2009) for example, Sedum alfredii (Crassulaceae) has been known to accumulate multimetal Cd, Pb and Zn, wherein Zn level reached less than 2% of shoot weight (Xiong et al., 2011). The phytoextraction method is highly economical, environment friendly with minimum disruption of soil compared to classical remediation approach (Mahar et al., 2016; Sheoran et al., 2016). The only limitation of this approach is dependency on the plants growing conditions, expertise of agricultural equipments and longer time period required to completely remediate the land. Hyperaccumulator plants have capability to accumulate 100 times higher concentration of metal than other plant species in natural environment. Depending on the type of heavy metals these plants are expected to accumulate 0.01%–1% of metals in their biomass (Raskin and Ensley, 2000; Brooks et al., 1998). Phytoextraction of heavy metals present in mine tailings faces several major challenges such as poor hyperaccumulation efficiency due to low metal bioavailability (Salt et al., 1995). Even if plant species are able to establish and survive in mining areas application of chelators are essential for accumulation of metals and biomass production (Berti and Cunningham, 2000; Krzaklewski and Pietrzykowski, 2002). Secondly, these areas face problem of metal solubility and results in leaching of metals in groundwater aquifers, mostly in temperate regions (Schmidt, 2003; Wu et al., 1999). (i) Pytoextraction in temperate environments Phytoextraction is challenging in mine tailings of temperate areas and faces problems of metal toxicity, acidic pH, poor soil structure, and low nutrient content. Plants tolerant to mine tailings mostly have low biomass production. T. caerulescens is identified to accumulate 50–160 mg kg−   1 Cd and 13,000–19,000 mg kg−   1 Zn when grown in mine tailings and mine spoils (Baker et al., 1994). T. caerulescens was also found to accumulate 8000 mg Zn and 250 mg Cd kg−   1 plant biomass in greenhouse study of mine spoil containing up to 3300 mg kg−   1 Zn and 58 mg kg−   1 Cd (Knight et al., 1997). However, T. caerulescens

Phytoremediation of abandoned mining areas for land restoration  43 showed low biomass production in mine tailings areas and require longer duration of 100– 1200 cropping cycles to remove Cd and 200–600 cropping cycles to remove Zn from affected mine sites. This study concluded that Cd/Zn hyperaccumulator may be effective in removal of moderately polluted area but is not recommended for highly contaminated mine spoils. Transgenic strains of B. juncea were reported to accumulate 1.5–3-fold higher concentration of metal (Cd, Cu, Cr, Pb, Zn) than wild type in a greenhouse study (Bennett et al., 2003). (ii) Phytoextraction in arid environment Soil in arid environment has less water content, acidic pH, and poor nutrient uptake rate. Numerous plants are observed to grow and colonize in arid atmosphere naturally but very few of them actually survived in greenhouse studies (Bech et al., 2002). Cichorium intybus and C. dactylon naturally colonize mine tailings in Spain and observed to accumulate 800–1500 and 400–1200 mg kg−   1 Pb in shoots. Shoot accumulation of Pb did not inhibit plant growth and biomass production in this study. Another study on Atriplex species is shown to accumulate high concentrations of Na and K in both noncontaminated soils and mine tailings (Mendez et al., 2007). In hydroponics greenhouse study, Atriplex halimus was reported to accumulate 830 and 440 mg kg−   1 of Cd and Zn in shoot biomass of plant with no visible symptoms of toxicity during growth (Lutts et al., 2004). Other study compared the accumulation of Cu, Pb, and Zn in Atriplex nummularia and Zea mays growing in 1:1 mixture of mine spoils and composted mulch (Jordan et al., 2002). In addition, metal chelator (EDTA) improved metal accumulation of Cu, Pb, and Zn to 400, 100, and 300 mg kg−   1, respectively.

2.5.2 Phytostabilization The main aim of phytostabilization is to prevent bioavailability and migration of pollutants into the groundwater or food chain by reducing their mobility (Erakhrumen, 2007). The heavy metals are restricted in soil near the roots but not in plant tissues mainly through precipitation (Bolan et al., 2011), complexation, or metal valence reduction in rhizosphere (Ghosh and Singh, 2005). The process also limits accumulation of heavy metals in biological structures and reduces their leaching into groundwater. This alternative phytotechnology generally employs extensive root system of native plants to restrict toxins in the surrounding plantation. The process successfully establishes plants and help to stabilize metals through precipitation into less soluble forms. It also enhances metal reduction, complexation of metals with organic products, metals sorption onto root surfaces and accumulation in root tissues (Cunningham and Ow, 1996; Wong, 2003). The establishment of plant cover on contaminated soil surface encourages diverse heterotrophic microbial community to promote plant growth and improved soil structure and quality (Mendez et al., 2007; Mummey et al., 2002; Wong, 2003). The established plant cover serves as the basis of successional development and self-sustaining system to minimize soil erosion and leaching. Naturally established plant communities on mine areas indicate the stability and

44  Chapter 2 diversity of plants that may vary upon regional basis because of different physicochemical factors, e.g., pH, cation exchange capacity, electrical conductivity and metal content (Conesa et al., 2007). Lime addition or organic amendments decrease metal availability in mine tailings for better plant establishment. As the metal mobility is restricted in phytostabilization, the ratio of shoot to root metal concentrations in soil should be   3000 mg/kg plant), significant amounts of Cu, Cr Pb, Ni, Zn, and a small amount of As (Álvarez-Mateos et al., 2019). High bioconcentration and low translocation factors were associated with remediation of Hgcontaminated soils by Jatropha (Marrugo-Negrete et al., 2015). In contrast, Yamada et al. (2018) reported that Jatropha does not hyperaccumulate potentially toxic elements (PTEs) such as Cd, Cr, Cu, Ni, and Zn but could be helpful in phytostabilization. On bauxite mine soil, J. curcas thrived well; thus, this plant is appropriate for phytoremediation of bauxite mine sites (Rahim et al., 2019). J. curcas has a great ability to tolerate and accumulate Al, Cu, Pb, Fe, and Zn in stem, roots, and leaves, indicating that this biodiesel plant is a suitable choice for phytoremediation of multimetal polluted lands (Majid et al., 2012).

3.2.2  Metal hyperaccumulator plants Metal accumulation in soil due to various natural and anthropogenic activities has significantly declined the fertility of soils. Most of the metals are not biodegradable and they are toxic to plants, animals, and humans; hence they should be removed from ecosystems. Phytoremediation, an eco-friendly method for removal of metal-contaminated sites is costeffective compared to other known remediation processes. Some plants can take up and accumulate valuable metals in their tissues in large quantities. Metal hyperaccumulator plants with high biomass generate significantly more income by utilizing metal-enriched biomass of plants in producing energy and recovery of metals. Phytomining involves recovery and extraction of valuable metals, Au, Ni, Fe, Zn, and Se from soil by harvesting high biomass hyperaccumulator plants. Nicks and Chambers (1995) reported for the first time that the use of Ni-hyperaccumulator Streptanthus polygaloides for phytomining of Ni at the US Bureau of Mines, Nevada with a yield of 100 kg sulfur-free Ni /ha. The high biomass plants A. bertolonii from Italy and B. coddii from South Africa are also promising candidates for phytomining (Robinson et al., 1997a,b). Potential use of B. coddii to remediate Ni polluted soil was assessed and it was projected that it could yield 100 kg Ni /ha at several sites worldwide. Robinson et al. (1997a,b) suggested that moderately Ni polluted soils (100 μg/g) could be remediated using only 2 crops of B. coddii. In fertilized (N and P amendments,) soils A. bertolonii produced dry biomass of 9 t/ha and 7 g Ni /kg, whereas B. coddii produced 22 t dry biomass/ha with 5 g Ni/kg dry biomass. It means A. bertolonii will require double the number of crops of B. coddii to phytoremediate mild Ni-polluted soils. Therefore, phytomining using B. coddii was proposed to be economically more beneficial. Energy generated from the combustion of the biomass of plants involved in phytomining further improved the economics of this operation

Efficient utilization of plant biomass  67 in a large-scale process (Brooks et al., 2001). Metals such as Ni, Pd, and Pt were efficiently extracted by B. coddii (Nemutandani et al., 2006). The mean concentration of Ni, Pd, and Pt in leaves was 13,980 ± 10,780, 0.22 ± 0.15 and 0.18 ± 0.07 mg/kg dry mass, respectively, whereas in roots it was 2046 ± 789, 0.14 ± 0.04 and 0.18 ± 0.07 mg/kg dry mass, respectively, and in the soil 1040 ± 686, 0.04 ± 0.03 and 0.07 ± 0.045 mg/kg dry mass, respectively. This results in a mean concentration of leaf to soil ratio of 13.4, 5.5, and 10.1 for Ni, Pd, and Pt, respectively. Mg, K, Na, S, and Ca also showed an average concentration ratio in the leaves to soil of around 2.5 or above. As the market value of Au is increasing continuously, phytomining of this metal is very beneficial (Sheoran et al., 2013). The potentials of desert willow to take up Au from Aurich media have been studied. Twenty to 80 mg Au/L did not affect the growth of the desert plant considerably. The concentration of Au in the plants increased as the age of the plant increased. Nearly 179 mg Au/kg dry weight was noted in the leaves of plants treated with 160 mg Au/L indicating the gold uptake potential of desert willow. Plants treated with 160 mg Au/L produced nanoparticles with an average size of 8 Å in roots, 35 Å in stems, and 18 Å in leaves. The average size was related to total Au concentration and their location in the plant (Rodriguez et al., 2007). Msuya et al. (2000) observed mean Au concentration of 48.3 mg/ kg dry weight in carrot roots in soil amended with chelating agents, ammonium thiosulfate and ammonium thiocyanate and concluded that the carrot is an economical crop to extract Au from mine tailings. Bio-assisted mining makes use of specially selected microorganisms to make metals available to hyperaccumulating plants from undissolved compounds (Maluckov, 2015). After extracting base metals from several plant harvests, microorganisms should be added that excrete cyanide to create chelates with gold. The combined use of microorganisms and plants is probably more effective than the application of plants or microorganisms only. Keeling et al. (2003) suggested a competition between Ni and Co for uptake and binding sites in roots. Bioaccumulation coefficients of Co and Ni (1000 μg/g) were 50 and 100, respectively (Keeling et al., 2003). They also showed the suitability of furnace treatment for getting Ni-rich bio-ore through hyperaccumulator plants. Reducing Ca uptake and/ or minimizing the content of Ca in the biomass before furnace treatment suggested this as a valuable strategy for refining Ni bio-ore quality generated in the phytomining process (Boominathan et al., 2004).

3.2.3  Aromatic and medicinal plants Since ancient times, aromatic and medicinal plants have been cultivated for a variety of uses. Nonedible aromatic plants are cultivated to get essential oils that are used in perfumes, cosmetisc, detergents, soaps, insect repellents, and food processing industries, whereas medicinal plants exhibit great medicinal and therapeutic properties. These plants, which

68  Chapter 3 are now considered as suitable candidates for phytoremediation, are nonfood crops which can be safely cultivated for remediation of polluted sites since they do not pose the risk of food chain contamination. They also do not get damaged or eaten by animals owing to their essence and they have monetary benefit due to valuable compounds obtained from them. Many medicinal and aromatic plants such as Vetiver (Vetiveria zizanioides), Madagascar periwinkle (Catharanthus roseus), geranium mint (Mentha sp.), peppermint (Mentha sp.), industrial hemp (Cannabis sativa), Tulsi (Ocimum basilicum), neem (Azadirachta indica), babool (Acacia nilotica), palmarosa (Cymbopogon martinii), citronella (Cymbopogon winterianus), lemon grass (Chrysopogon zizanioides), East-Indian lemon grass (Cymbopogon flexuosus), lemon grass (Cymbopogon citratus), Castor (Ricinus communis), marijuana (Cannabis sativa), etc., are tolerant to stress and thus, phytoremediation using these plants are ecologically feasible and viable (Jisha et al., 2017). Aromatic plants belonging to the Families Lamiaceae, Asteraceae, Poaceae, and Geraniaceae appear to be promising for heavy-metal phytoremediation from the contaminated sites. They have the potential to act as hyperaccumulators, phytostabilizers, facultative metallophytes, and bio-monitors (Pandey et al., 2019). They can be grown in marginally polluted soils where food crops cannot be grown. Many of these plants can tolerate and extract toxic metals such as Cd, Cu, Ni, As, Fe, etc., from the contaminated land. Heavy metal increases the percentage of essential oil of some aromatic plants (Pandey et al., 2019). After oil extraction, the residual biomass can be used for the production of energy either by direct burning or gasification of biomass. Thus, this integrated approach has the potential for oil production and to mitigate several environmental issues such as greenhouse gas reduction and pollution alleviation. (Pandey et al., 2019). Azadirachta indica (Neem) and Vachellia nilotica (babool) show phytoremediation capability accompanied by great medicinal and therapeutic properties. Neem extract shows antibacterial, antiinflammatory, antipyretic, antiarthritic, antigastric (ulcer), spermicidal, hypoglycaemic, antifungal, diuretic, antimalarial, antitumor, and immunomodulatory properties, whereas babool is used to treat diarrhea, excessive bleeding, diabetes, gonorrhea, eye-watering, fever, dysentery, leucorrhoea, and blood clotting. Also, energy-efficient biodiesel of international standards can be obtained from these tree species (Tiwari et al., 2017). Cat’s Whiskers, a valuable medicinal plant used in traditional folk medicine has demonstrated cardioactive, antiinflammatory antioxidant, antidiabetic, hepatoprotective, antigenotoxic, antiplasmodic, cytotoxic, and antimicrobial activities. It is also considered as a good phytoremediator species, particularly for Zn and Pb. Heavy metals taken up by this plant accumulated primarily in leaves, indicating that it has the potential to phytoremediate heavy metals (Arifin et al., 2011). Madagascar periwinkle, a valuable medicinal plant used in Wilms tumor, leukemia, malignant lymphomas, Hodgkin disease, Kaposi sarcoma, neuroblastoma, mycosis, fungoides, and high blood pressure, absorbs up to around 38% of Cr from the soil via roots and accumulates around 22% in leaves and hence could be used in the remediation of

Efficient utilization of plant biomass  69 Cr-contaminated land (Ahmad and Misra, 2014). Hemp, which shows medicinal properties, can remove toxic metals from polluted sites, produces high biomass, and can be used for producing bioenergy. Leaves of hemp plants grown on contaminated sites accumulated 1530 mg Cu/kg, 151 mg Cd/kg, and 123 mg Ni/ kg, indicating the efficiency of hemp plant to tolerate the metals (Ahmad et al., 2016). Ocimum basilicum (Tulsi) is a well-known plant with great medicinal properties such as antiseptic, antibacterial, antipyretic, antifungal, antioxidant, and anticancer. Tulsi seedlings, which showed tolerance to Cr, when treated with different concentrations of Cr (0–8 mg/L) showed the highest concentration of Cr in roots (8 mg/L) and less amount of Cr transportation to shoots. Vetiver grass is commonly used as a tonic, blood purifier, and to treat skin disorders. High biomass, wide roots, and environmental tolerance of this plant make it potential species for phytoremediation (Das et al., 2010; Datta et al., 2011, 2013). Datta et al. (2013) observed tetracycline accumulation in the root and shoot and noted complete removal of tetracycline from the soil in 40 days using this plant. Vetiver grass possesses a high affinity for 2,4,6 trinitrotoluene (TNT). At 40 mg/kg soil-TNT concentration, complete removal was observed by vetiver in presence of urea (Das et al., 2010). Vetiver grass can tolerate moderate levels of As (up to 225 mg/kg) and accumulates As from soils contaminated with pesticides (Datta et al., 2011). It has been shown to possess tolerance to high concentrations of Pb in soils. Further, the addition of EDTA significantly increased Pb translocation from roots to shoots. Chen et al. (2004) showed that vetiver planted in soil matrix could re-adsorb 98%, 88%, 54%, and 41%, of the originally applied Pb, Cd, Cu, and Zn, respectively, which may decrease the hazard of the downward flow of heavy metals and entrance in the groundwater. Medicinal plant hemp shows high tolerance to metals and can accumulate Cd, Ni, and Cr when grown in soils S1 and S2 containing 126, 74, and 27 μg/g of Cr, Cd, and Ni and 139, 115, and 82 μg/g of Cr, Cd, and Ni, respectively. One ha hemp biomass (about 10 t) appears to extract a considerable amount of Ni and Cd per year and with time a gradual restoration of deep soil can be attained via its extensive root system. Hence, a better quality of soil can be obtained along with an economical advantage (Citterio et al., 2003).

3.2.4  Ornamental plants Ornamental plants that are used for beautifying gardens and landscapes can also be used for the removal of contaminants. Several ornamental plants grow well in te contaminated soils polluted with heavy metals and organic compounds (Liu et al., 2017). Typical ornamental species Tagetes patula, Mirabilis jalapa, Calendula officinalis, and Althaea rosea possess the capability to phytoremediate oil-contaminated sites. A significant reduction of Total Petroleum Hydrocarbons (TPH) was observed in 10,000 mg/kg of the TPH-polluted soil (Liu et al., 2012). Tagetes patula has been suggested to have the potential for remediation of benzo[a]pyrene [(B[a]P)] and B[a]P–Cd contaminated sites (Sun et al., 2011). The average

70  Chapter 3 removal rate Mirabilis jalapa of petroleum from polluted soil in Shengli Oil Field, China was 41.61%–63.20% using Mirabilis jalapa compared to 19.75%–37.92% by natural attenuation. The saturated hydrocarbon fraction was reduced more compared to other fractions of petroleum pollutants (Peng et al., 2009). A combined Medicago sativa and F. arundinacea (Fire Phoenix) are excellent plant species for the remediation of polycyclic aromatic hydrocarbon-contaminated soils (Xiao et al., 2015). Ornamental plants such as Althaea rosea and Calendula officinalis are promising candidates for Cd phytoremediation (Liu et al., 2008). Application of Egtazic Acid (EGTA) and Sodium Dodecyl Sulfate (SDS) increased biomass and promoted the accumulation of Cd in roots and shoots (Liu et al., 2008).

3.3  Methods for effective use of biomass of phytoremediator plants obtained during growth and after harvesting If biomass obtained during and after the phytoremediation process is left unattended, it can result in secondary pollution (Ali et al., 2013; Song and Park, 2017). Therefore, it is essential to efficiently use and manage this biomass. Using metal hyperaccumulators, aromatic, and bioenergy plants for phytoremediation, it has been possible to use the biomass for getting valuable metals, essential oils, and bioenergy.

3.3.1  Bioenergy production Burning of fossil fuel releases a high amount of CO2, leading to global climate change (Rotty and Masters, 1985; Wuebbles and Jain, 2001; Höök and Tang, 2013) and the continuous depletion of stored fossil fuel is a major challenge (Dresselhaus and Thomas, 2001; Höök and Tang, 2013). Therefore, there is a great need to look for renewable alternative energy resources (Dresselhaus and Thomas, 2001). Plant biomass generated from the phytoremediation process can be utilized for bioenergy production (Van Ginneken et al., 2007; Gomes, 2012; Jha et al., 2017). Biomass is one such important resource (Klass, 1998; Cheng, 2018) and it can be utilized to regenerate transportation fuels, thermal energy, or renewable electricity (Balat et al., 2009). Biomass is usually defined as a freshly dead or living plant or animal and any by-product derived from these organisms. Living biomass utilizes carbon for growth and this carbon is released when it is used for energy (Searchinger, 2010). Biomass to bioenergy conversion can be done in two ways: (i) thermo-chemical processes such as direct combustion, pyrolysis, distillation, gasification, and liquefaction; and (ii) biological processes such as anaerobic bio-gasification, bio‑hydrogen production and alcoholic fermentation (Balat et al., 2009; Zhang et al., 2010) (Fig. 3.3). Direct combustion of wood chips, pellets, and other dry biomass is used to generate thermal energy at the level of the personal building. First-and second-generation biofuels (FGB and SGB) such as bioethanol, biogas, and biodiesel can be generated from phytoremediator plant biomass (Hill, 2009; Gomes, 2012; Jha et al., 2017). Biomass consisting mainly of highly digestible sugars such as sugarcane

Efficient utilization of plant biomass  71

Fig. 3.3 Bioenergy produced from bioenergy crops used for phytoremediation.

can be easily transformed into bioenergy by the process of fermentation and distillation (monosaccharides and disaccharides). The production of bioenergy using wheat and corn starch, which are composed of amylose and amylopectin, begins with enzymatic hydrolysis to convert them to monosaccharides (glucose) (Weislogel et al., 1996). Breaking of α-1,6-glycosidic branch points present in amylopectin is difficult compared to the β-1,4-glycosidic bond. Generation of ethanol using biomass needs wide processing to liberate the polymeric sugars in hemicellulose (23%–53%) and cellulose (20%–35%). Cellulose, where glucose monomers are linked through β-1,4-glucosidic linkages, is a linear polysaccharide, whereas hemicelluloses are highly branched chains consisting of arabinose and xylose and they also contain galactose, mannose, and glucose (Weislogel et al., 1996). Cellulose hydrolysis involves the degradation of cellulose polymer into simpler sugar molecules and therefore it is a critical step involved in the generation of biofuel. Acidogenesis leads to the formation of sugars and volatile fatty acids are produced from long-chain fatty acids, and generating CO2 and/or hydrogen and acetic acid from volatile fatty acids (Den et al., 2018). Acetic acid generated during acetogenesis can be converted into CH4 and CO2, a process known as methanogenesis. Fermentative bacteria can also lead to CH4 production from fatty acids and amino acids. Fermentation of saccharin materials such as fructose, glucose, and sucrose mediated usually by yeasts leads to ethanol and CO2 production (Weislogel et al., 1996; Demirbas, 2005; Den et al., 2018).

72  Chapter 3 Phytoremediator plants belonging to second-generation biofuel (lignocellulosic biomass) usually consist of hemicellulose, cellulose, and lignin and are therefore valuable biopolymers for the generation of energy (Robak and Balcerek, 2018). Currently, comparatively less bioenergy is generated from lignocellulosic biomass than feedstock like starch and sugarcane because lignin is a recalcitrant component, making bioenergy production difficult despite the existence of rich chemical functional groups (Den et al., 2018). It is composed of polyphenols which are linked by an intricate net of phenyl propanoic monomeric units with diverse inter-unit bonds. It cross-links hemicellulose and cellulose, hence making cell walls rigid and three-dimensional (Whetten and Sederoff, 1995). Hardwood usually contains less lignin compared to softwood and agricultural residues usually contain even lower concentrations of lignin and are therefore more suitable for bioenergy production. Lack of valorization of lignin is associated with chemical heterogeneity. Since it is second in order of abundance of biopolymers and constitutes 15%–30% of the biomass, lignocellulosic biomass pre-treatment is important for the production of energy (Alvira et al., 2010). Various pretreatment technologies are available for the production of bioethanol based on enzymatic hydrolysis (Alvira et al., 2010). They result in detachment of lignin from hemicelluloses and cellulose and depolymerization of the cellulose and lignin, hence increasing the surface area of carbohydrates for enzymatic saccharification. Hemicellulases and cellulolytic enzymes are used for effective saccharification and produce a wide variety of sugars, mainly glucose and xylose in the hydrolysate which can be converted into ethanol by microorganisms (Khare et al., 2015). Mmicroorganisms such as Candida shehatae, Pachysolen tannophilus, and Pichia stipites transform xylose to ethanol (Sanchez et al., 2002). Genetic engineering can be used to confer microorganisms with the capability to ferment pentose (i.e., xylose) accumulated in hydrolysates (Sharma et al., 2014). Sharma et al. (2018) showed the assimilation of xylose in S. cerevisiae LN that could be enhanced by adaptive evolution and suggested its possible commercial utilization. Biomass obtained from phytoremediator plants can be exploited to generate bio-oil, a potential alternative energy source that can be converted to biodiesel and used as a fuel in diesel engines, boilers, or gas turbines for electricity generation and heat production (Bauddh et al., 2015). There are primarily two processes through which biomass can be converted to bio-oil: hydrothermal liquefaction and pyrolysis (Xiu and Shahbazi, 2012; Gollakota et al., 2018). In the process of pyrolysis, biomass is degraded using heat in the absence of O2, producing bio-oil (liquid), charcoal (solid), and fuel gas, whereas in the hydrothermal liquefaction process medium-temperature and high-pressure are applied to produce bio-oil (Toor et al., 2011). Microwave irradiation and ultrasound processesusing milder advanced catalytic and oxidative processes are now being examined as an efficient replacement for pyrolysis and hydrothermolysis that use harsher acid and alkaline treatments (Den et al., 2018). Bio-oil is converted into biodiesel through a trans-esterification reaction in which alcohol combines with an ester to make another alcohol and ester. Fats and oils belonging to

Efficient utilization of plant biomass  73 the ester family unite with ethanol/methanol to generate ethyl or methyl esters and glycerol in the presence of a catalyst, methoxide (Leung et al., 2010). Anaerobic fermentation of plant biomass generated from the phytoremediation process can lead to the production of eco-friendly biogas that mainly contains methane and CO2 (Chynoweth et al., 2001). Methane is the key constituent of biogas (50%–85%) and represents the key energy source utilized in boilers for heat production. In the case of woody biomass, hemicelluloses and cellulose are considered to be the main sources of methane, whereas lignin, which is not degraded in the absence of O2, does not produce methane (Sawatdeenarunat et al., 2015). Different physical, chemical, and biological pre-treatments are available for the delignification of biomass (Nakamura and Mtui, 2003). Anaerobic fermentation involves a chain of biochemical reactions carried out by different microbes of various metabolic groups such as methanogens, acidogens, hydrolytic bacteria, and acetogens that result in methane or biogas generation (Ziemiński and Frąc, 2012). Among these microbes, a syntropic relation exists to generate final products, CO2 and methane. They mutually rely on one another for energy. Biochemical reactions during the anaerobic digestion can be classified into two key steps: (i) production of acid and (ii) acid transformation to methane. The differential rate of these biochemical reactions leads to acid buildup, which can decrease the pH and constrains the process, mainly the methanogenesis. Ammonia, organic acid, and sulfide generated in the anaerobic digestion process can also serve as inhibitors.

3.3.2  Extraction of heavy metals Phytoextraction, which is an environmentally-friendly method for cleaning heavy-metal polluted soils, generates heavy-metal-enriched biomass as secondary waste (Keller et al., 2005). Problems related to the disposal of these plants pose difficulties in the use of this technique. Therefore, the efficient utilization of contaminated biomass obtained during and after the remediation process is necessary. Valuable metals such as Au, Cu, Ni, Tl, Ag, Fe, etc., can be extracted from phytoremediator plants. The two most frequent methods employed for this purpose are dry ashing and wet oxidation. Keller et al. (2005) suggested incineration as a feasible possibility for metal extraction from the heavy-metal-contaminated plant biomass. A reactor (laboratory scale) was made to simulate the evaporation behavior of metals in the furnace and volatilization of metals from plant biomass samples was examined using a thermo-desorption spectrometer. A study done at the temperature ranging from 25°C to 95°C with Thlaspi caerulescens (Cd and Zn hyperaccumulator) and Salix viminalis (high biomass) grown in metal-contaminated soils revealed that pyrolysis, which occurs under reducing conditions, is a better process compared to incineration, which requires oxidizing conditions, for increasing volatilization; the subsequent recovery of Cd and Zn occurs from the plant biomass that also allows bottom ash recycling as fertilizer (Keller et al., 2005). The incineration of plant biomass is progressively used for heat production

74  Chapter 3 and/or electricity. Once incinerated, bottom ash (coarser) and fly ash (finer) are obtained. Bottom ashes contain important elements for plants and low levels of metals and therefore can also be used as fertilizer. Since fly ashes contain high heavy-metal concentration, they are major environmental pollutants and hazardous in the absence of expensive emission controls (Carević et al., 2017). Lievens et al. (2008) studied the effect of pyrolysis temperature and the type of solid heat carrier (fumed silica and sand) on heavy-metal concentration in the ash/char fraction of sunflower and birch biomass contaminated with Cd, Cu, Pb and Zn, obtained from phytoremediation after thermal treatment and suggested that selection of proper thermal conditions for maximum recovery of metals is necessary. Kröppl and Lanzerstorfer (2013) tried to clean fly ash containing high concentration of metals by extraction using hydrochloric acid. The heavy metals were separated by sodium hydroxide precipitation. They suggested that after cleaning, ash could be pelletized and added to soils. One of the possible solutions for fly ash management is the utilization of fly ash in the construction industry, particularly the concrete industry (Carević et al., 2017). Biomass combustion was designed to get Ni salt from Ni hyperaccumulator plants growing in serpentine soils. The valorization of Ni was done by the pyro- or hydrometallurgical process. Key parameters that affected the quality of ashes were duration and temperature. The best conditions for obtaining good quality ashes were using 550°C temperature for 3 h. Ashes obtained in this way contained Ni concentration of 20 wt%. Valuable metals could be recovered from biomass ashes (Zhang et al., 2014). For the extraction of gold, biomass is first ashed, dissolved in 2 M HCl, and then the solvent is extracted in methyl isobutyl ketone (MIBK). The application of sodium borohydride (reducing agent) to the organic layer results in black precipitates at the boundary between the layers. The heating of precipitates at 800°C leads to the formation of metallic gold (Lamb et al., 2001). Germanium (Ge), a metalloid that is mainly recovered during the extraction of Zn as a by-product has great industrial application as a semiconductor. Since global mining of Zn is declining, this can create a problem for Ge production also. Ribbon grass (Phalaris arundinacea) is found to possess the capability of accumulating Ge from Gecontaminated soils such as mine tailings. After harvesting, Ge-enriched plants can be used for the production of bioenergy and geranium extraction. In the PhytoGerm project, a method for extraction of Ge was developed that was based on leaching and distillation of Ge using HCl (Rentsch et al., 2016). Distillation leads to the extraction of Ge as germanium tetrachloride (GeCl4) from the fly ash mixture. As there is a step of solid–liquid separation, recycling of HCl can be done using a feed of fresh HCl, the molarity of the solution can be adjusted. GeCl4 obtained is then injected in a second reactor with sodium hydroxide (NaOH) solution for the precipitation of germanium (IV)-oxide, which is subsequently separated by filtration. This process ends with the generation of powdery germanium (IV)-oxide. Further reduction of oxide to Ge metal powder can be done in ultra-clean graphite boats at 760°C (Melcher and Buchholz, 2014).

Efficient utilization of plant biomass  75

3.3.3  Essential oil extraction Plant-based essential oils are volatile and can be used in the food and perfume industries. They also help to fight against bacterial pathogens in low doses (Akhtar et al., 2014; Oussalah et al., 2007) mainly due to various active phytochemicals and compounds present in them. Azeotropic distillation (steam distillation, hydrodistillation, and hydrodiffusion) and solvent extraction are common processes used for extraction of essential oil from the plants (Rassem et al., 2016). Hydrodiffusion, another method of extracting essential oil, differs from steam distillation in the way steam is fed. In the hydrodiffusion method, the steam is supplied from the top instead of from the bottom as done in steam distillation. Cold pressing or scarification method is another common technique and one of the best methods for isolation of essential oils. In this method, without enhancing the temperature, the pressure is applied to the plant sample that is in contact with the solvent (Ferhat et al., 2007). The plant material is pressed to discharge the essential oil, which rises to the surface and is isolated from the material using centrifugation (Rassem et al., 2016). Another conventional solvent extraction method is based on solid–liquid extraction in which solvent (hexane, dimethyl ether, methanol, ethanol, or other solvents that can dissolve essential oils) passes through the solid matrix in which solute gets dissolved and diffuses out. Any factor such as solvent property, the ratio of solvent to solute, temperature, or duration, which can enhance the diffusion and solubility, can assist the extraction process (Zhang et al., 2018). Due to the several drawbacks in conventional methods such as low yields, by-products formation, thermally unstable compound degradation due to temperature and unsaturated compounds and hydrolytic effects, the focus is now for the search of more rational methods for extraction (De Castro et al., 1999). Elyemni et al. (2019) applied two different processes, hydrodistillation and microwave-assisted hydrodistillation (MAH), to extract essential oils from the plant Rosmarinus officinalis and concluded that MAH possesses considerable benefits compared to conventional hydrodistillation. The yield and aromatic profile of essential oils obtained through Microwave hydrodiffusion and gravity (MHG) for 15 min from pennyroyal (Mentha pulegium) and spearmint (Mentha spicata) were similar to essential oil obtained after hydrodistillation for 90 min (Vian et al., 2008). Sometimes undesirable compounds are produced in microwave-assisted extraction (MAE) and superheated liquid extraction (SLE) due to toxicity of organic solvents and very high temperature. Ultrasoundassisted extraction (USAE) is faster, more efficient, more cost-effective, and does not need high temperature or polar extractants (Vilkhu et al., 2008). However, during the process of sonolysis of the solvent, there are chances of producing free radicals that can degrade some unstable compounds via oxidation. Supercritical fluid extraction (SFE), which can be performed at relatively low temperatures, makes use of extractants such as nontoxic and chemically inert CO2 (Sapkale et al., 2010). However, high purity CO2 is required because of the affinity of CO2 for impurities with low-polar and nonpolar compounds present in

76  Chapter 3 the sample. Twelve compounds were obtained from Nepeta persica in the steam-distilled oil. However, only two components contained greater than 90.0% of the oil obtained using supercritical CO2 under optimum conditions. Using steam distillation 0.08% (v/w), extraction yield was obtained, whereas by SFE extraction 0.22%–8.90% (w/w) yield could be obtained (Khajeh et al., 2010).

3.4  Conclusions and future prospects Phytoremediation is progressively emerging as a safe and sustainable process for remediation of polluted sites. The cost associated with this method is generally lower compared to other remediation approaches. Phytoremediation also provides the prospect of enhancing the financial opportunity using plants that can be utilized to produce bioenergy, aromatics, medicines, decorative materials and recovery of valuable metals through phytomining. The utilization of contaminated residual biomass of phytoremediator plants for energy production leads to a reduction of secondary pollution. Identifying phytoremediator plants with economic benefits and then improving their performance through conventional plant breeding and genetic engineering approaches are needed to reduce contamination of polluted sites and enhance income generation too.

Acknowledgments PS acknowledges DST-Science and Engineering Research Board (SERB) project no. ECR/2016/000888 and UGC-Start-up grant no. F.4-5(107-FRP)/2014(BSR) for financial support. KB acknowledges DST-SERB New Delhi, India for financial support (EEQ/2017/000476).

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CHAPTE R 4

Characteristics of mining spoiled and oil drilling sites and adverse impacts of these activities on the environment and human health Lala Saha and Kuldeep Bauddh Department of Environmental Sciences, Central University of Jharkhand, Ranchi, Jharkhand, India

4.1 Introduction Mineral resources have been exploited by human beings for thousands of years to obtain precious metals for their use and economic value. The mining sectors remained comparatively small until the industrial revolution and following technological advancement. Overshoot in growth and opulence of the human population increased the demand for several materials, especially elements such as gold, silver, iron, aluminum, crude oil, and coal (Johnson, 2003; Elshkaki et al., 2018; Lèbre et al., 2019). At the same time, the mining activities unpredictably affect the environment by altering its physical, chemical, and biological properties, affecting all living organisms, including human beings (Fazekašová and Fazekaš, 2020; Mishra and Das, 2020; Prematuri et al., 2020). The mining of metals and coals generate a tremendous amount of waste materials. It may consist of the spoil heap, ruin building, and used as offsite dumping sites or fly-tipping. These metals are stored into large heaps or mounds on the ground for further treatment or for landfills. The waste material or the by-products of heaps are highly variable that contain several chemically reactive and inert components (Nawab et al., 2015; Ding et al., 2017; Fazekašová and Fazekaš, 2020; Prematuri et al., 2020). These reactive components run off with the rainfall or get leached into the soil and many times up to the groundwater (Luís et al., 2011; Cidu et al., 2012; Pourret et al., 2016). Another endemic problem with the abandoned mine sites is the formation of acid discharge water, which is composed of a significant amount of dissolved iron sulfate and a variety of heavy metals (HMs) and metalloids (Gilchrist et al., 2009; Cidu et al., 2012).

Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00020-0 © 2021 Elsevier Inc. All rights reserved.

87

88  Chapter 4 Most importantly, the environmental concern depends on the type of mining method and the geographical location of the mining sites (Mhlongo and Amponsah-Dacosta, 2015). For example, surface mining causes different land disturbances than those by the underground mining process. Several case studies show that mining abandoned sites caused problems for the local environment. For example, abandoned copper mines named Mynydd Parys situated in the United Kingdom remains barren due to the toxic effects of weathering surface materials (Johnson, 2003). The study found that the dominant minerals found in the ore are galena (PbS), chalcopyrite (CuFeS2), pyrite (FeS2), and sphalerite (ZnS). The most common problems of abandoned mine sites are the alteration of the landscape, change in soil properties, harsh pH level, unused shafts and pits change in surface and groundwater regimes, subsidence, sites become derelict, change in vegetation cover, etc. (Mhlongo and Amponsah-Dacosta, 2015; Jain and Das, 2017) (Fig. 4.1). Apart from environmental concern, mining affects the socioeconomic status of the local communities. During the setup of mine activity, it brings a lot of investment that benefits the local communities through creating job opportunities, developing new infrastructures such as drinking water, electricity, healthcare, and schools. The socioeconomic opportunities open new ways to settle new communities around the mine sites; thus, the mine sites get densely populated many times. But once the mines get abandoned, the stressed environmental conditions adversely affect the quality of life and livelihood of the local people (Mhlongo and Amponsah-Dacosta, 2015).

4.2  The type and characteristics of mining dumping sites The nature and condition of mining dumpsites depend on the kind of materials mined, the process used, the time scale of locations, pollution control efforts, and the environmental factors (Zabowski et al., 2001; Jahanshahi and Zare, 2015). Mining dumpsites can be characterized by the elevated concentration of various metals such as As, Cd, Cr, Cu, Mn,

Fig. 4.1 Problems related to mining.

Characteristics of mining spoiled and oil drilling sites  89 Ne, Pb, and Zn and radioactive substances. The dumpsite soil supports a severely stressed heterotrophic microbial community because of its different soil structure compared to its normal soil structure (Mendez et al., 2007; Chaturvedi et al., 2012). In many mining abandoned sites, reactive sulfide mineral compounds are to be found as a common component. The sulfidic minerals remain stable in dry and oxygen deficiency areas, but when exposed to water and oxygen, they are oxidized spontaneously. Sulfide mineral oxidative dissolution process is quite a significant topic because during this process sulfide may divide into acid-soluble minerals (Johnson, 2003). The minerals which are acid-insoluble and can be oxidized by ferric iron in acid liquors are solubilized with the help of iron-oxidizing bacteria. For example, acid-soluble sulfide such as sphalerite is attached by protons as follows Eq. (4.1) (Johnson, 2003). (4.1) ZnS  2H   Zn 2   H 2 S The hydrogen sulfide (H2S) oxidized by sulfur-oxidizing microorganisms as in Eq. (4.2). (4.2) H 2 S  2O2  2H   SO 4 2  The acid-insoluble sulfide minerals such as chalcopyrite and pyrite reaction with ferric iron produced ferrous iron, thiosulfate, and protons as follows FeS2  6 Fe 3  3H 2 O  7Fe 2   S2 O32   6H  The minerals present in the heaps tend to be very heterogeneous and have different chemical characteristics within short distances. In the case of coal and mineral spoils, heaps containing a high amount of sulfidic minerals may generate high temperatures due to exothermic oxidation reactions. In the utmost case, the result is the spontaneous combustion of spoil coal heaps and may last for many years (Mhlongo and Amponsah-Dacosta, 2015). Apart from coal and metals, other mining activities generate different constituents of mining dumpsites, which are discussed in the following section separately.

4.2.1  Coal mining Coal mining operations generate a considerable amount of rocks (discarded mine stone), rejecting coal and fines that are produced during washing. These material excavation from the anoxic subsurface and transfer to the surface for the process. Residues from the mining contain various metals like Al, Cu, Fe, Mn, Pb, Zn, etc. (Silva et al., 2013). The acid drainage from the abandoned coal mine contains a large amount of solid in suspension, sulfate, and dissolved metals that contaminate the surface and underground water. This problem can persist for centuries after the mine abandonment. Various environmental issues due to the coal mining activities become a serious concern threatening the ecology of the mining area (Shi and He, 2012). The topsoil of coal mining areas gets blended with overburden materials

90  Chapter 4 and loosely packed soil may affect the soil physicochemical properties (Pandey et al., 2014). The dust particle generated in the coal mining areas acts as the epicenter for many chemical reactions. The spontaneous heating of coal in waste dumping sites causes the fire to release a substantial amount of SO2. During this combustion process, the atmospheric nitrogen binds with the oxygen to form NOX. A study done by Shi and He (2012) reported that major pollutants from the coal mining, solid waste comprises 3.6 million tons, composed; 0.012, 0.048, 0.3,0.78, and 2.46 million tons of dust, sulfur dioxide, gangue, sewage, and concentrator waste, respectively. It is also reported that about 3.55 million tons of gangue accumulated over the year in the study site. Acid mine discharge (AMD) also causes serious concern in the coal mine abandoned sites. The AMD happens when the pyrite reacts with air and water, which formed H2SO4 and dissolved iron. The acid dissolves HMs such as Cu, Hg, Pb, which may mix with surface and groundwater. It estimated that in the United States, there are over 1.1 million surface acres of abandoned coal mines, over 900 miles of polluted streams by AMD, and many miles of unsafe highwalls, surface impounds, and embarkments (Zhengfu et al., 2010).

4.2.2  Crude/mineral oil Abandoned crude oil mining sites include old mines, processing units, equipment and tools, oil wells, and buildings. The products of crude oil represent one of the most common environmental contaminants. Drilling waste sump and flare pits are excavated, where the waste disposed during the well drill, acts as a source of contamination (Thiessen and Achari, 2017). Abandoned mining sites may have had emergency earthen pits for storing the waste saltwater generated during hydrocarbon-producing formation. Source of contamination also depends on the well type, type of fluid storage, and well maintenance activities that occur at the well site (Thiessen and Achari, 2017). Studies show that crude oil is composed of 10, 000 different hydrocarbons, which are highly toxic and can cause severe damage to the aquatic ecosystem (Dawes, 1998; Ifelebuegu et al., 2017). Pollutants such as polyaromatic hydrocarbons (PAHs), short-chain alkanes, HMs, oil, and grease are introduced into the coastal and marine environment. The contaminants such as HMs accumulated in the aquatic and terrestrial environment can disrupt the ecosystem (Bhattacharya et al., 2016; Ifelebuegu et al., 2017). The bitumen from the oil sands processes to synthetic crude oil, which is chemically different from the crude oil and contains a higher concentration of metals and sulfur. The study found that the diluted bitumen can contain a high amount of Cu, Ni, and Pb than the conventional crude oil, and also contain a large amount of other hazardous pollutants like benzene (Finkel, 2018). Despite bitumen’s reputation of being a dirty fuel, industries are continuously mining, extracting, and processing the oil-rich bitumen, which is further refined into gasoline or asphalt. Primarily bitumen extraction takes place in two ways; i.e. in-situ mining, and open-pit mining. In-situ mining is applied when bitumen lies in depth. During the drilling, the steam is injected in both the

Characteristics of mining spoiled and oil drilling sites  91 methods to heat the bitumen, making it more fluid and to flow freely. The bitumen is then pumped out to the ground. But in the case of open-pit mining/surface mining produced a large amount of liquid tailing, which is toxic. The tailing is then stored into the tailing pond. An example has been seen in Alberta, Canada, where 30 mile2 of tailing ponds were leaching toxic chemicals that threaten the environment and people living there (Gosselin et al., 2010; Finkel, 2018).

4.2.3  Bauxite mining Mining of bauxite being an impermanent activity, most of the time, negatively impact the environment in long terms. In terms of production, the primary source of the world’s aluminum comes from bauxite as 99% of metallic aluminum (Lee et al., 2017). The bauxite is extracted from both surface and underground deposits. Surface mining is more common than underground mining because most of the bauxite deposits occur near the surface. The extraction of bauxite takes place by shallow, open-cut mining following the open-pit method. The bauxite ores content is of different types and the most amount of clay, and need to be washed before the process (Donoghue et al., 2014; Lee et al., 2017). It is naturally occurring heterogeneous material, composed of one or many aluminum hydroxide minerals such as boehmite [γ-AlO(OH)], diaspore [α-AlO(OH)]4, gibbsite [Al(OH)3], and other compounds such as hematite [Fe2O3], quartz [SiO2], kaolinite [Al2Si2O5(OH)4], goethite [FeO(OH)], and rutile/anatase [TiO2] with a trace amount of impurities (Lee et al., 2017). Trace elements found in bauxite include As, Cd, Cr, Mn, Hg, Pb, Ni, and radioactive materials such as uranium and thorium. These toxic substances are often found in bauxite residues, even after the extraction of aluminum. A study done by Callisto et al. (1998) showed that the bauxite mining effluent from Mineracao Rio do Norte S/A contains 7% to 9% of the finely grounded solid particle, mainly aluminum oxide (21%), silicate (4%), and iron oxide.

4.2.4  Iron ore mining Iron ore is another important mineral from which metallic iron is extracted. The high demand for metal leads to continuous mining and processing, generating a large amount of solid and liquid waste. From the beginning of extraction to processing and at the final stages, it generates a hefty amount of tailing, which contains various toxic metals such as Fe, Mn, Cu, Pb, Co, Cr, Ni, and Cd (Diami et al., 2016). It is estimated that almost 32% of iron ore extracted end up as tailing (Ghose and Sen, 1999). Iron ore mining sites, and the wastewater tailing generated from it, contain high level of dissolved iron and particulate suspended matter which alter the water chemistry and bioavailability of metals (Holopainen et al., 2003; Pereira et al., 2008)

4.2.5  Copper and manganese mining The mining of Cu leaves a legacy of metalliferous materials, which include rock waste, rockfill, and tailing (Owor et al., 2007). During the process of Cu from the Cu-coralliferous pyrite, ores generate a huge amount of waste. The waste materials are composed of sulphidic components and when it is exposed to the environment, it leads to oxidation, resulting in acid

92  Chapter 4 rock drainage (ARD) and AMD. The increase in acidity mobilized the sulfates and metals such as Cu, Cr, Pb, Co, Zn, and Ni in the surrounding area, which alter the physicochemical properties of the surrounding environment. Mn ore mining, smelting, and processing involve crushers, screens, scrubbers, and spiral classifier. In the process, the coarse fractions are separated, which contain a high concentration of Mn and the fine particles discarded as tailings. The tailings from the Mn mining contain HMs such as Mn, Cd, Pb, Cu, Ni, and Zn (Wang et al., 2018).

4.2.6  Uranium mining The uranium (U) is mined through three processes, underground, surface, and solution mining (in situ leaching). The underground and surface mining generates waste which consists of overburden soil, rocks, and trace amounts of ore with radioactive decay products. The mining also includes the extraction of U from the ore by physical and chemical methods. Each step of U processing generates radioactive wastes that contain naturally occurring radioactive elements (Abdelouas, 2006). The highest volume of tailing comes from mine and mill processing. The U mining tailing also contains an elevated concentration of toxic metals such as As, Pb, Cd, and Zn which are the primary sources of surface and groundwater pollution (Abdelouas, 2006; Lind et al., 2013).

4.3  Environmental contamination from mining 4.3.1  Impact on the air contamination The majority of mining activities contribute to air pollution directly and indirectly. The foremost source of air pollution in mining areas are blasting, drilling, grinding, cutting, loading and unloading of raw materials, loss from overburden truck during transportation, wind erosion from exposed dumping sites, and emissions from diesel and petrol engines (Chaulya, 2004; Lee et al., 2017). The primary air pollutants generated from the mining activities are total suspended particulate matter (SPM), particulate matter (PM2.5 and PM10), oxides of nitrogen (NOx), oxide of sulfur (Sox), and other gaseous pollutants (Chaulya, 2004). The dust particles generated from mining introduced into the atmosphere act as the center of catalysis, where the number of chemical reactions occurs (Ghose and Majee, 2000). The dust generated from bauxite mining is detrimental because it reduces visibility and results in visual changes to the environment (Petavratzi et al., 2005).

4.3.2  Impact on water contamination Water pollution due to mining activities is another important environmental concern. When the contaminated water from the mining sites enter into the aquatic ecosystem, it affects the aquatic life, agriculture, and fresh drinking water, due to high concentration

Characteristics of mining spoiled and oil drilling sites  93 of toxic substances (Monjezi et al., 2009; Yi et al., 2011; Shaari et al., 2015). In minewaste, AMD formation can interact with the naturally available carbonate, and salts result in altering the pH level in natural waters (Monjezi et al., 2009). The mining activities have also been reported to increase the turbidity of water (Mertzanis, 2012). Metals such as Cd, Cr, Hg, Ni, Mn, and Fe leached out into the groundwater. These HMs are mobilized in water, flowing to down streams and deposited into the clay minerals, which are further absorbed by the algae (Bradl, 2005). As the metals get accumulated into the primary producer, they passed from one trophic level to another, and caused the problem of biomagnification, thereby causing toxicity to the top consumers. Several studies highlighted the mining activities impact on water resources, which have been tabulated in the following section (Table 4.1). Table 4.1: Impact of mining activities on water. Mining type/sites

Contaminants

Coal mining area

Cd, Cr, As, Li, Ba, Be, Sr, B, Ag, Co, Cu, Fe, Mn, Ni, Zn, Al, Bi, Pb, and Ti

Bauxite mine

Cd, Cr, Pb, Ni, As, Mn, Co, Cu, Sr, and Zn

Bauxite mine

Hg, Al, and Fe

Iron ore mine area

Mn, Co, Ni, Pb, Mo, Sr, Al, As, B, Cu, Ba, U, Fe, and Zn

Iron-ore mining

As, Cr, Cu, Pb, Ni, Hg, Fe, and Mn

Remarks

References

The concentration of As, Fe, Al, Mn Singh et al. (2017) in pre-monsoon and Ba, Pb, Mn, and Ni in post-monsoon seasons exceeds the permissible limits of Indian drinking water standards The study found that the water Kusin et al. (2017) quality index of some study areas was polluted and the concentration of metal contents exceeded the recommended permissible limits The water collected from the Abdullah et al. (2016) nearby residential area found higher concentration Al(0.20 mg/L) than health ministry level and Hg (0.0093 mg/L) was nine times higher than the recommended level for raw water The metals such as Al, As and Mn Jahanshahi and Zare mean concentration in groundwater (2015) samples recorded above the WHO maximum permissible limits for drinking water. Despite the concentration of these metals exceeded the permissible limits, the indices showed most of the water samples are moderately polluted and overall contamination levels are out of danger The study found that mining Pereira et al. (2008) activities were the potential sources of Cr, Cu, As, Pb, Ni, Hg, Mn, and Fe

94  Chapter 4

4.3.3  Impact on soil and soil microorganism From the beginning of mining, the soil and natural ecology of the area gets disturbed by various activities like clearing the land before mining, the opening of new roads, deforestation and construction of waste disposal sites, etc. These activities change the soil physical, chemical, and biological properties like loss of soil structure, increased bulk density, low water holding capacity, a decrease of organic matter, altered pH, and reduction of microbial diversity and their activities (Šourková et al., 2005; de Quadros et al., 2016; Feng et al., 2019; Fazekašová and Fazekaš, 2020; Prematuri et al., 2020). In post-mined soil, the organic matter content is usually less due to high disturbance in topsoil, which leads to lowered nutrient availability for the microbial community. This results in a decrease in soil microbial diversity and soil functional stability (de Quadros et al., 2016). The mining activities affect the soil microbial communities, which may cause a negative impact on the biogeochemical cycles (de Quadros et al., 2016). It is seen that after coal mining, the soil surface gets contaminated with pyrite (FeS2) and in later stage oxidized to sulfuric acid when it comes in contact with the water and oxygen results to a high level of soil acidification (de Quadros et al., 2016). Prasad et al. (2012) stated that HMs like Cd present in mining soil affect the free-living nitrogen-fixing bacteria such as Azotobacter spp., which reduced their diversity, abundance, and concurrent soil health. Various studies have been conducted to know the mining effects on soil properties and their associated living organism have depicted in Table 4.2.

4.3.4  Impact on plants There are a large number of studies, which found that the HMs negatively variously affect the plants (Lewis et al., 2001; Yadav, 2010; Hasan et al., 2017; Liu et al., 2018; Goyal et al., 2020) (Table 4.3). The contaminants from the mining areas enter the food chain via various routes and cause acute and chronic adverse effects on animals and plants. The dust generated from the mining sites affects the plant’s physiological process such as growth, productivity, and reproduction capability. When the contaminants entered the plants, alter the plant’s physicochemical activities. HMs such as As and Ni reduced the chlorophyll and carotenoid concentration in plants (Mascher et al., 2002; Shaibur et al., 2009).

4.3.5  Impact on human beings People residing near the mining areas get affected by physical, chemical, and biological hazards associated with mining processes. Physical hazards include noise, vibration, heat, ultraviolet radiation, and humidity; chemical hazards include harmful gases such as methane, carbon dioxide, sulfur dioxide, and toxic metals; and biological hazards include

Characteristics of mining spoiled and oil drilling sites  95 Table 4.2: Effects of mining contaminants on soil and soil microorganism. Mining sites

Analysis of parameters/ types

Copper tailings subdams

Soil physicochemical properties and microbial diversity

Coal mining

Microbial diversity and biomass

Coal mine area

Earthworm diversity

Cu-Zn-Pb mine

Soil enzyme activities, microbial biomass C, N, and P (MBC, MBN and MBP) basal respiration, qCO2, and N mineralization Soil microbial diversity and activity

Copper mining wasteland

Remarks

References

The study found that bacteria are affected more than fungi. The study also confirmed that significant negative correlations between catalase and the soil carbon and nitrogen ratio As compared to undisturbed sites, the mining areas recorded substantially lower microbial diversity and biomass, with less activity of β-glucosidase and dehydrogenase enzymes The study recorded that species richness was highest in undisturbed areas (average 10 sp. per area) while very low recorded in the mining area (average 1.33 sp. per area) The result showed that the presence of Cd, Pb, Cu, and Zn in mining soil leads to a decrease in soil enzyme activities, MBC, MBN, MBP, N mineralization, and increase in qCO2and basal respiration

Jia et al. (2019)

The important microbial parameters such as the ratio of microbial biomass C (Cmic)/organic C (Corg) and microbial quotient (qCO2) were affected by the presence of HMs in the mining site

de Quadros et al. (2016)

Boyer et al. (2011)

Zhang et al. (2010)

Liao et al. (2005)

tropical diseases like malaria, dengue, fever, and another bacterial and fungal disease like leptospirosis and ancylostomiasis (Donoghue, 2004; Donoghue et al., 2014; Wesdock and Arnold, 2014). The dust particles generated from the mining areas irritate the eyes, throat, and nose and contaminates the water and food sources. The dust particles settle down in the surrounding vegetation and make them unpalatable for human beings (Abdullah et al., 2016). Particulate matters like PM10 and PM2.5 generated from the mining areas cause various respiratory and cardiovascular diseases. The contaminants absorbed by the aquatic animals, plants, and terrestrial vegetation enter the human body through the food chains that cause severe health problems (Bradl, 2005; Yi et al., 2011; Petavratzi et al., 2005). The contamination of HMs such as Pb, Cd, As, Hg, Cr, Mn, and Cr can cause various diseases like damage to the central and peripheral nervous system, impaired neurocognitive function, hypertension, cardiovascular disorders, nephrotoxicity, kidney and bone diseases, low birth rates, dermatological manifestation, cancer, hearing loss and increase in mortality (Nawrot et al., 2006; Ahern et al., 2011; Bernhoft, 2012; Flora et al., 2012; Wright et al.,

96  Chapter 4 Table 4.3: Effects of mining contaminants on plants. Heavy metal present in common mining sites Chromium (Cr)

Mercury (Hg)

Lead (Pb)

Nickel (Ni) Manganese (Mn) Zinc (Zn)

Copper (Cu)

Effect on plant

References

Higher amount of Cr results in chlorosis in young leaves, root injury, imbalanced nutrient, inhibition of plant growth, and wilting of tops Ionic form of Hg, i.e., Hg2  + acts as phytotoxic to plant cells. It can induce physiological disorders (oxidative stress) and visible injuries in plants Pb causes harmful effects on growth, photosynthetic processes, and morphology. The higher concentration of Pb causes inhibition of enzyme activities, change in membrane permeability, water imbalance, and interrupts mineral nutrition Ni2  + causes chlorosis, necrosis, osmotic imbalance, and decreased photosynthetic activity Mn toxicity results in necrotic lesions, crinkle and browning leaf, and death The high concentration of Zn inhibited plant metabolic functions which control plant growth and chlorosis occur in younger leaves Cu produced a cytotoxic role, which causes stress and injury to plants. It controls plant growth and occurs in chlorosis

Scoccianti et al. (2006); Yadav (2010) Zhou et al. (2007)

Sharma and Dubey (2005); Yadav (2010)

Rahman et al. (2005); Sachan and Lal (2017) Wu (1994); El‐Jaoual and Cox (1998) Ebbs and Uchil, 2008

Lewis et al. (2001)

2012; da Rosa Couto et al., 2018). High level of Al works as neurotoxin and link to Alzheimer’s disease, also associated with bone diseases in children (Flaten, 2001; Abdullah et al., 2016; Lee et al., 2017). Excess iron contaminated can cause chronic ingestion, hepatic disease, diabetes, cardiomyopathies, and hyper-pigmentation (Lee et al., 2017). The high concentration of Zn can cause various health problems such as skin irritation, vomiting, anemia, stomach cramps, and nausea and affect growth and reproduction (Larakeb et al., 2017). Asbestosis, silicosis, pneumoconiosis, siderosis, asthma, and even lung cancer are the common chronic diseases occurring in people residing close to the mining areas.

4.4  Social impact of mining Mining has both positive and negative social impacts. It all depends on the types of methods used for mineral extraction, the mining site’s location, mining duration, and the size of the mining area. Large-scale mining activities lead to significant demography changes, which cause structural and functional aspects of the local social environment (Petrova and Marinova, 2013). Several studies highlighted the social impacts on various aspects in terms of economy, income and security, land use and terrestrial aspects, employment and education, demography and human rights issues, and environmental health and safety issues (Loayza and Rigolini,

Characteristics of mining spoiled and oil drilling sites  97 2016; Mancini and Sala, 2018). In the case of the economy, it stimulates the local economy, increases the income of people, and opens new business opportunities in other sectors. Its negative impact includes income inequality in terms of unfair distribution of benefits from resource extraction and corruption due to poor management trigger social tension. Many other impacts negatively affect the livelihood of rural people, the cultural degradation of indigenous people, and the discrimination of valuable groups. After the mining, the alteration of the landscape, generation of wasteland, and, in some cases, lowering the groundwater table caused long-term problems to the local communities.

4.5 Conclusion The extraction of essential metals and other valuable substances like coal, oil, and natural gas is needed for a nation for its growth in all respects like economic, social, and cultural. Mining activities enhance job opportunities to the local peoples, health facility, education, etc. Simultaneously, due to the adoption of non-sustainable processes, mining activities release a huge amount of liquid, solid and gaseous contaminants that disturb the air, water, and soil ecosystems. Toxic metals, solid debris, acids, radioactive materials, etc. are common harmful substances released from the mining sectors. Mining activities are also responsible for the loss of natural habitat, loss of soil fertility, enhanced soil erosion, forced migration of tribal communities, etc. Continuous research and updates in the mining processes must be done to minimize the adverse impacts caused. The application of environment-friendly tools must be adopted for the extraction of essential components.

Acknowledgment Authors are thankful to the Science and Engineering Research Board (SERB), New Delhi, India for the award of a research grant (EEQ/2017/000476).

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CHAPTE R 5

Phytorestoration of abandoned ash-ponds by native algal strains Alka Kumari Department of Botany, University of Lucknow, Lucknow, India

5.1 Introduction The majority of power generating stations are coal-based in India (Khan and Khan, 1996), which estimate to produce around 140 million ton fly ash (FA) during 2020 (Kalra et al., 1998), which cause contamination of both soil and aquatic ecosystems. A 200-MW thermal power plant generates approximately 300 tons of FA per day. Since coal-based power plants produce a huge amount of FA as a byproduct (residue) that contains several inorganic compounds, noxious metals, and metalloids and becomes a potential source of pollution. Its management has been considered a very important element in terms of environmental perspective. FA contains several valuable metals and metalloids such as, Hg, Al, Cd, Pb, Cr, and As, which may be recovered by using suitable plant species. If not recovered/removed from the sites, many of these heavy metals become toxic and can cause serious health hazards like renal failure, major symptoms of chronic toxicity, and liver damage (Andrew et al., 2003; Shaw et al., 1997). Although FA produced from thermal power plants is being used in various construction activities including landfilling and query restoration but even then, a large quantity of the ash remains for eco-friendly management. Therefore, the only cost-effective and eco-friendly solution suggested for the management of FA is revegetation of the landfill area by the FAtolerant plants, which served the purpose of stabilization and provides a pleasant landscape (Adriano et al., 1980; Wong and Wong, 1990; Vajpayee et al., 2000; Rai et al., 2004). Phytoplanktons are able to accumulate a significant amount of heavy metals from the contaminated surface water and already reported as bioindicators and phytoremediators of heavy metals from polluted water bodies. Algae play an important role in maintaining the equilibrium of the aquatic ecosystem and also as good indicators of water pollution. They are also useful for environmental monitoring as phytotoxicity tests (Boswell et al., Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00005-4 © 2021 Elsevier Inc. All rights reserved.

105

106  Chapter 5 2002). Several cyanophycean algae have been reported to accumulate significant amounts of toxic metals from FA contaminated surface water (Rai et al., 2000; Mohamad, 2001; Rai et al., 2005). Green algae (GA) also absorb heavy metals from the contaminated environment (Rai and Chandra, 1992; Terry and Stone, 2002). The dominance of algal species (both green and blue-green algae (BGA)) in Ganga water polluted through leaching of FA and heavy metal accumulation by Phormedium papyraceum from FA has also been reported by Dwivedi et al. (2006) and Dwivedi et al. (2008), respectively. Some microalgal strains are also able to accumulate chromium and other heavy metals from polluted sites (Dwivedi et al., 2010). Various phycological studies in different localities of Bhagalpur districts of Bihar have also been done time to time (Singh and Saha, 1982a, b; Saha, 1985, 1986; Saha and Pandit, 1987; Saha and Wujek, 1989; Kumar and Saha, 1993; Kargupta and Jha, 2004). Recently extensive floristic survey of algal flora in Vikramshila Gangetic Dolphin Sanctuary of Bhagalpur, Bihar has been carried out by Das and Maurya (2015) and water quality and phytoplanktons of Gandak river have also been done by Kumar and Choudhary (2016). Recently studies on “Algae as a green technology for heavy metals removal from various wastewater” has been reported by Salama et al. (2019) and in the same year another report on “Techno-economic estimation of wastewater phycoremediation and environmental benefits using Scenedesmus obliquus microalgae” has also been reported by Ansari et al. (2019). The more recent paper on “Marine Algae as Natural Indicator of Environmental Cleanliness” has been reported by Parus and Karbowska (2020). According to Yoon et al. (2006), species growing naturally on a contaminated site respond better under stress conditions than plants introduced from other areas in terms of their suitable establishment in a changed environment. Besides, the species obtained from such contaminated sites might possess greater potential of metal and metalloid accumulation. Therefore, the present work has been carried out to identify heavy metal sensitive and tolerant native algal species and their accumulation potential growing in contaminated sites to use them for amelioration of soil and water quality as well as eco-restoration purposes of such abandoned ash ponds. The study also included the analysis of physicochemical properties of contaminated water bodies and its corelation with algal diversity, density, and metal content in high biomass producing algal species collected from the selected sites.

5.2 Methodology 5.2.1  Sampling sites The study was conducted on different water bodies in the vicinity of National Thermal Power Corporation (NTPC) Kanti, Muzaffarpur (Bihar), India. During the study, three water bodies were selected for sampling according to their distance from FA dumping sites as well as at different pollution levels viz. highly polluted sites (HPS) (inside ponds of campus area within 1 km), moderately polluted sites (MPS) (inside ponds of the residential area around 2 kms),

Phytorestoration of abandoned ash-ponds by native algal strains  107 least polluted sites (LPS) (village area of Kusi around 3 kms). These water bodies were denoted as HPS, MPS, and LPS, respectively.

5.2.2  Characterization of physicochemical studies of the selected water bodies and effluents Water samples (250 mL) were collected in triplicate from each site in plastic containers. Surface water qualities were monitored for each site and temperature was also measured on spot by a thermometer. Dissolved oxygen (DO), pH, electrical conductivity (EC), and total dissolved solids (TDSs) were analyzed by a portable Water Analysis Kit (Century CMK, 731), while other parameters like biochemical oxygen demand (BOD), chemical oxygen demand (COD), and phosphorus were estimated as per procedures given in (APHA, 1985).

5.2.3  Collection and characterization of algal strains The phytoplankton and biomass of the algae were collected from water bodies using Wisconsin plankton net (28 μm mesh) and preserved in 250 mL plastic bottles with the help of sterilized forceps inside formaldehyde. The material was examined immediately after bringing it to the laboratory in living conditions and photomicrographs were taken with a Nikon microscope SZ1450. The occurrence frequency of algal species was determined using a hemocytometer based on the percent occurrence of an individual species by considering the total no. of species present in the samples. Individual algae species were classified as dominant (>  70%), common (40%–70%), and rare ( Oscillatoria >  Oedogonium > Hydrodictyon > Cymbella. But the trend was slightly different for copper as.

Phytorestoration of abandoned ash-ponds by native algal strains  111 Table 5.3: Heavy metal accumulation by different algal strains growing in fly ash polluted water bodies in the vicinity of NTPC-Kanti, Muzaffarpur, Bihar. Species name Anabaena doliolum

Phormedium papyraceum

Oscillatoria nigra

Nostoc muscorum

Hydrodictyon reticulatum

Oedogonium capitellatum

Spirogyra longata

Navicula cryptocephala

Cymbella affinis

Site details HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS HPS MPS LPS

Different metals & metalloids accumulated by algal strains (μg/g) Fe 921 ± 98 668 ± 73 446 ± 55 896 ± 74 635 ± 55 416 ± 39 699 ± 81 568 ± 73 436 ± 59 776 ± 71 585 ± 63 436 ± 49 679 ± 62 589 ± 58 476 ± 44 687 ± 67 518 ± 59 426 ± 42 886 ± 89 768 ± 85 586 ± 56 785 ± 61 568 ± 43 ND 656 ± 65 365 ± 34 ND

Cu

Zn

Ni

Cr

Cd

As

98 ± 7.6 69 ± 4.3 57 ± 2.2 75 ± 4.5 56 ± 3.6 47 ± 1.5 54 ± 2.7 38 ± 1.4 31 ± 1.2 69 ± 3.6 44 ± 2.6 38 ± 1.4 64 ± 3.5 41 ± 1.3 26 ± 1.1 55 ± 2.2 38 ± 1.5 22 ± 1.2 89 ± 2.5 43 ± 1.6 36 ± 1.5 61 ± 3.6 37 ± 1.5 ND 57 ± 2.7 38 ± 1.4 ND

72 ± 5.7 61 ± 3.5 52 ± 2.4 67 ± 1.5 51 ± 0.5 36 ± 1.3 37 ± 1.5 24 ± 0.5 BDL 79 ± 6.5 50 ± 2.5 BDL 54 ± 1.6 33 ± 0.5 27 ± 1.1 52 ± 1.7 30 ± 1.5 26 ± 0.5 56 ± 1.5 36 ± 0.6 BDL 47 ± 1.2 28 ± 0.7 ND 42 ± 1.5 24 ± 1.1 ND

59 ± 2.6 48 ± 2.1 35 ± 1.5 49 ± 2.5 36 ± 1.6 27 ± 1.5 39 ± 2.7 28 ± 1.4 21 ± 1.2 55 ± 3.5 34 ± 2.6 28 ± 1.4 44 ± 1.5 31 ± 1.3 26 ± 1.1 45 ± 2.2 38 ± 1.5 22 ± 1.2 67 ± 2.1 43 ± 1.6 36 ± 1.5 52 ± 1.6 37 ± 1.5 ND 47 ± 1.7 33 ± 1.4 ND

47 ± 3.5 29 ± 1.6 BDL 41 ± 2.3 25 ± 1.2 BDL 31 ± 1.3 23 ± 1.1 BDL 39 ± 2.5 22 ± 1.5 BDL 15 ± 0.3 BDL BDL 18 ± 1.3 11 ± 0.5 BDL 34 ± 2.3 21 ± 1.5 BDL 32 ± 1.3 13 ± 0.3 ND 27 ± 1.5 11 ± 0.3 ND

27 ± 1.2 15 ± 0.3 BDL 24 ± 0.5 17 ± 1.1 BDL 18 ± 1.5 12 ± 0.4 BDL 21 ± 1.3 13 ± 0.3 BDL 16 ± 0.5 09 ± 0.2 BDL 15 ± 1.5 05 ± 0.2 BDL 11 ± 1.5 03 ± 0.1 BDL 20 ± 0.5 15 ± 1.2 ND 17 ± 2.5 BDL ND

22 ± 1.1 11 ± 0.5 BDL 19 ± 0.3 09 ± 0.2 BDL 13 ± 0.2 BDL BDL 16 ± 1.2 07 ± 0.5 BDL 12 ± 0.3 05 ± 0.1 BDL 05 ± 0.5 01 ± 0.1 BDL 13 ± 1.2 04 ± 0.5 BDL 15 ± 0.3 08 ± 0.4 ND 06 ± 0.3 03 ± 0.1 ND

Mean ± SD (n = 3, student’s t-test significant (P  > Spirogyra > Phormidium > Nostoc > Navicula > Hydrodictyon >  Oscillatoria  > > Oedogonium > Cymbella. Trends for other metals like Zn, Ni, Cr, Cd and As are as follows: Zn—Nostoc > Anabaena > Phormidium > Spirogyra ≫ Hydrodictyon > Oedogonium >  Navicula > Cymbella > Oscillatoria. Ni—Spirogyra > Anabaena ≫ Nostoc > Navicula > Cymbella > Oedogonium >  Hydrodictyon > Oscillatoria > Phormidium. Cr—Anabaena > Phormidium > Nostoc > Spirogyra > Navicula > Oscillatoria >  Cymbella > Oedogonium > Cymbella > Hydrodictyon. Cd—Anabaena > Phormidium > Nostoc > Navicula > Oscillatoria > Cymbella >  Hydrodictyon > Oedogonium > Spirogyra.

112  Chapter 5 As—Anabaena > Phormidium > Nostoc > Navicula > Spirogyra  >  Oscillatoria >  Hydrodictyon >  Oedogonium > Cymbella. As per the above trends, it is notable that most of the toxic metals like Cr, Cd, and As have almost similar trends of accumulation like Anabaena is most accumulator strain followed by Phormidium, Nostoc, Navicula, Spirogyra, and others. However, in the case of essential elements like Fe, Cu, Zn, and Ni the trends are changed. For Fe and Cu Anabaena is the top accumulator but in the case of Zn and Ni Nostoc and Spirogyra are top accumulators respectively. Similar results were obtained by Rai and Chandra (1992) and Rai et al. (2000).

5.4 Conclusion In conclusion, the result showed that most of the algal species perform high population density with a better growth rate on metal-polluted water bodies without any visible toxicity symptoms. Moreover, different algal species accumulated a significant amount of heavy metals in highly polluted sites followed by moderately polluted and least polluted sites. Anabaena and Phormedium species have extraordinary accumulation capacity of almost all tested metals. Besides, other algal strains like Nostoc, Spirogyra, Navicula, and some other BGA and GA are also capable of metal accumulation. As metal-polluted sites (coming with FA) are nitrogen- and phosphorus-deficient, in such cases BGA may prove to be an excellent successor due to its potential ability to maintain soil fertility, organic matter, soil moisture, and nitrogen fixation. Overall, the results indicate that these native algal strains are highly suitable candidates for amelioration as well phytorestoration of FA polluted abandoned ponds/dykes. However, further studies on metabolic adaptation of target algal species are required to understand its internal mechanism of defense system against toxic metals. There is a high possibility to use such algal strains for phycorestoratoration of abandoned coal mines also.

Acknowledgments The author is thankful to late Dr. P.S. Ahuja, Former DG, CSIR New Delhi and Director CSIR-IHBT, Palampur for extending required laboratory/research facilities and Dr. M.R. Susheela, former Senior Principal Scientist, CSIRNBRI, Lucknow for identification of algal species. Thanks are also due to DST for financial support because this work is additional data of my previous project under the WOS-A Scheme (SR/LS/WOS-117/2008).

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Phytorestoration of abandoned ash-ponds by native algal strains  113 Ansari, F.A., Ravindran, B., Gupta, S.K., Nasr, M., Rawat, I., Bux, F., 2019. Techno-economic estimation of wastewater phycoremediation and environmental benefits using Scenedesmus obliquus microalgae. J. Environ. Manag. 240, 293–302. APHA, 1985. Standard Methods of Water and Wastewater Analysis. APHA, Washington, DC. Boswell, C., Sharma, N.C., Sahi, S.V., 2002. Copper tolerance and accumulation potential of Chlamydomonas reinhardtii. Bull. Environ. Contam. Toxicol. 69, 546–553. Das, S.K., Maurya, O.N., 2015. Floristic survey of Algae in Vikramsila Gangetic Dolphin Sanctuary, Bihar (India). Nelumbo 57, 124–134. https://doi.org/10.20324/nelumbo/v57/2015/87116. Desikachary, T.V., 1959. Cyanophyta. ICAR Monograph on Blue Green Algae. Indian Council of Agricultural Research, New Delhi. Dwivedi, S., Srivastava, S., Mishra, S., Dixit, B., Kumar, A., Tripathi, R.D., 2008. J Hazard. Mater. 158 (2–3), 359–365. https://doi.org/10.1016/j.jhazmat.2008.01.081. Dwivedi, S., Tripathi, R.D., Rai, U.N., Srivastava, S., Mishra, S., Shukla, M.K., Gupta, A.K., Sinha, S., Baghel, V.S., Gupta, D.K., 2006. Dominance of algae in Ganga water polluted though fly-ash leaching: metal bioaccumulation potential of selected algal species. Bull. Environ. Contam. Toxicol. 77, 427–436. Dwivedi, S., Srivastava, S., Mishra, S., Kumar, A., Tripathi, R.D., Rai, U.N., Dave, R., Tripathi, P., Charkrabarty, D., Trivedi, P.K., 2010. Characterization of native microalgal strains for their chromium bioaccumulation potential: phytoplankton response in polluted habitats. J. Hazard. Mater. 173, 95–101. Gomez, K.A., Gomez, A.A., 1984. A Statistical Procedure for Agricultural Research. John Wiley & Sons, New York. Kalra, N., Jain, M.C., Joshi, H.C., Choudhary, R., Harit, R.C., Vatsa, B.K., Sharma, S.K., Kumar, V., 1998. Fly ash as a soil conditioner and fertilizer. Bioresour. Technol. 64, 163–168. Kargupta, A.N., Jha, R.N., 2004. Algal Flora of Bihar (Zygnemataceae). Bishen Singh Mahendra Pal Singh, Dehradun. Khan, M.R., Khan, M.W., 1996. The effect of Fly-ash on plant growth and yield of tomato. Environ. Pollut. 92, 105–111. Kumar, B.N., Choudhary, S.K., 2016. Water quality and phytoplankton of river Gandak, Bihar (India). Pollut. Res. 35 (1), 167–176. Kumar, S., Saha, L.C., 1993. Fresh water algae of drinking water reservoirs at Bhagalpur. Phykos 32, 131–146. Mohamad, Z., 2001. Removal of Cd and Mn by a non-toxic strain of the fresh water cyanobactrium Gloeothece magna. Water Res. 35, 4405–4409. Parus, A., Karbowska, B., 2020. Marine algae as natural indicator of environmental cleanliness. Water Air Soil Pollut. 231. https://doi.org/10.1007/s11270-020-4434-0. Philipose, M.T., 1967. The Chlorococcales. ICAR Publication, New Delhi. Prescott, G.W., 1951. Monograph Algae of the Western Great Lakes Area. Cambrook Institute of Science, Michigan. Rai, U.N., Chandra, P., 1992. Accumulation of Cu, Pb, Mn, and Fe by field population` of Hydrodictyon reticulatum (Linn.) Lagerheim. Sci. Total Environ. 116, 203–211. Rai, U.N., Tripathi, R.D., Kumar, A., Ali, M.B., Pal, A., Singh, N., Singh, S.N., 2000. Bioremediation of fly ash by selected N2 fixing blue green algae. Bull. Environ. Contam. Toxicol. 64 (2), 294–301. Rai, U.N., Pandey, K., Sinha, S., Sinha, A., Saxena, R., Gupta, D.K., 2004. Revegetating fly ash landfills with Prosopis julifora L.: impact of different amendments and Rhizobium inoculation. Environ. Int. 30, 293–300. Rai, U.N., Dwivedi, S., Tripathi, R.D., Shukla, O.P., Singh, N.K., 2005. Algal biomass: an economical method for removal of Cr from tannery effluent. Bull. Environ. Contam. Toxicol. 75, 297–303. Saha, L.C., 1985. Periodicity of algal flora in Bhagalpur ponds in relation to ecological factors. J. Ind. Bot. Soc. 64, 25–30. Saha, L.C., 1986. Algae of Bhagalpur ponds—Bacillariophyceae. Phykos 25, 136–143. Saha, L.C., Pandit, B., 1987. Pond and riverine algae of Bhagalpur. Phykos 26, 152–158. Saha, L.C., Wujek, D.E., 1989. Phytoplankton distribution in an oligotrophic pond and a eutrophic pond. Acta Hydrochem. Hydrobiol. 17, 407–416. Salama, E., Roh, H., Dev, S., et al., 2019. Algae as a green technology for heavy metals removal from various wastewater. World J. Microbiol. Biotechnol. 35. https://doi.org/10.1007/s11274-019-2648-3.

114  Chapter 5 Shaw, D., Leon, C., Kolev, S., Murray, V., 1997. Traditional remedies and food supplements. A 5-yeartoxicological study (1991–1995). Drug Saf. 17, 342–356. Singh, N.K., Saha, L.C., 1982a. Diatoms of Bhagalpur ponds. I. Bihar. Phykos 21, 128. Singh, N.K., Saha, L.C., 1982b. Chlorococcales of Bhagalpur—1, Bihar. J. Econ. Taxon. Bot. 3, 197–200. Terry, A.P., Stone, W., 2002. Biosorption of Cd and Cu contaminated water by Scenedesms abundans. Chemosphere 47, 249–255. Vajpayee, P., Rai, U.N., Choudhary, S.K., Tripathi, R.D., Singh, S.N., 2000. Management of fly ash landfills with Cassia surattensis Burm: a case study. Bull. Environ. Contam. Toxicol. 65, 675–682. Wong, J.W.C., Wong, M.H., 1990. Effects of fly ash on yields and elemental composition of two vegetables, Brassica parachinensis and B. chinensis. Agric. Ecosyst. Environ. 30, 254–264. Yoon, J., Cao, X., Zhou, Q., Ma, L.Q., 2006. Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci. Total Environ. 368, 456–464.

CHAPTE R 6

Mine tailings phytoremediation in arid and semiarid environments Elizabeth J. Lama, Ítalo L. Montofréb,c, and Yendery Ramíreza,d a

Chemical Engineering Department, Universidad Católica del Norte, Antofagasta, Chile bMining Business School, ENM, Universidad Católica del Norte, Antofagasta, Chile cMetallurgical and Mining Engineering Department, Universidad Católica del Norte, Antofagasta, Chile dSchool of Engineering Science, Lappeenranta-Lahti University of Technology, Lappeenranta, Finland

6.1 Introduction Generally, copper is distributed occupying large surfaces, often mixed with other minerals in the rocks. As a result, the production process faces complex and growing challenges that increasingly requiring technological complexity. The mineral has lost significant value over the past two decades due to resource depletion and a decrease in the relationship between mineral and sterile material converging towards lower grade ore. Chile is one of the major copper producers on the planet, where copper is one of the raw materials with the highest industrial use, and it has multiple applications, which entails a high economic benefit for the country. However, like all industrial activities, it has generated environmental impacts of several kinds, wherein the largest ones correspond to mine tailings (Mendez and Maier, 2008; Orchard et al., 2009). Mine tailings pH ranges from 2 to 9, depending on the acid-generating potential and carbonate content (Mendez and Maier, 2008). Mine tailings occupy large areas of soil and cause severe environmental impacts, either because of its toxicity and concentration or due to its interaction with environmental factors such as oxygen and water (Kossoff et al., 2014). These wastes are constituted by ground rock, minerals, sand-sized particles, or silt, lack nutrients to support biological growth with roughly no organic matter, contain water (Ye et al., 2002; Rosario et al., 2007; Mendez and Maier, 2008; Santibañez et al., 2012; Babel et al., 2016; Wang et al., 2017), heavy metals, and chemicals such as CN−, As, Pb, Cd, Zn, Hg, among others, a product of the mineral processing (Mendez and Maier, 2008). Metal concentrations concerning As, Cd, Cu, Mn, Pb, and Zn can range from 1 g kg−  1 in modern mine tailings to 50 g kg−  1 in historic mine tailing (Lam Esquenazi et al., 2018; Lam et al., 2019).

Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00012-1 © 2021 Elsevier Inc. All rights reserved.

115

116  Chapter 6 Mine tailings have high heterogeneity and complexity depending on their physical, chemical, and mineralogical properties and also on environmental factors where they are located, and on natural phenomena that could influence their behavior, such as torrential rainfalls or high magnitude seismic events, becoming a constant threat. As mentioned previously, each tailing is unique, and, therefore, its response is also specific, which makes it very complex to develop an effective policy for all of them that contain management tools applicable to each tailing. Since the technological advance has allowed the development of new and more efficient technologies that will allow us to extract higher amounts of valuable elements, such as copper, gold, iron, and Rare Earths, the interest on old tailings, whose mineral grade could be of economic importance, has emerged. Some of these elements have a high demand for industrial applications. However, these tailings could also contain high concentrations of dangerous elements or compounds, either by themselves, or by reactions between them or by reactions with water and air, and may generate higher risks. Therefore, it is crucial to develop proper management of tailings, especially those that are abandoned, for reasons of safety for people as well as for the environment (Lam et al., 2019). Mining and metallurgical industrial waste results in the ecosystem contamination with heavy metals of soil, landscape, vegetation, and human health. The mine waste impacts can be classified into landscape, flora and fauna, soil, water, and human health. Some consequences result in adjustments in the landscape, habitats destruction, soil and water pollution, degradation of land resources, acid mine drainage (AMD) generation, sedimentation and erosion processes, discharge metals and metalloids, among others (Acosta et al., 2018). The large tailing volume produces a significant environmental footprint for storage, considering spatial and temporal aspects (Adiansyah et al., 2015). Other significant ecological damages involve air contamination by toxic air emissions, particulate matter, depletion, and contamination of surface and groundwater resources (Lam et al., 2016). The world’s annual mine tailings discharge exceeds 10 billion tons (Adiansyah et al., 2015). Annually, Chile generates over 500 million tons of tailings, placing this country as the third-largest accumulator of these wastes after China and the United States. The increased production projection is expected by 2035, the volume of tailings being doubled (CESCO, 2019). Currently, Chile has 6500 million m3 of tailings, and for projects and expansion, it has approved over 14,470 million m3 (SERNAGEOMIN, 2019). In Chile, there is a large amount of Mining Environmental Liabilities (MEL) distributed throughout the country, within which the majority corresponds to tailings. The National Geology and Mining Service (SERNAGEOMIN, 2019), carried out cadasters on tailings deposits in the country, where the last cadaster made in December 2018 revealed the presence of 742 deposits, of which only 104 are active, and the rest are inactive, a large part of the latter is abandonment in a state. Where the State of Chile must take care of the abandoned tailings, therefore, it is necessary to obtain the best technologies to remediate and stabilize.

Mine tailings phytoremediation in arid and semiarid environments  117 Historically in Chile, tailings were neglected without appropriate management because of inadequate legislation. Residuals that have been called MEL are generally the result of mining operations that were neglected or paralyzed without an adequate closure plan. According to Yupari (2003), the denomination of MEL refers to the negative impacts caused by abandoned mining operations, with or without a distinguishable proprietor, and where a legalized mine closure has not been carried out and authorized by the authority. MEL is also an extensive reference to those impacts that can be caused by waste (solids, liquids, and gaseous) generated during the different phases of the mining process. Currently, Chilean regulation entails that tailings should be physically and chemically stabilized (Lam et al., 2016, 2019). Mining operators are obligated to present a closure plan that ensures the stability of mine tailings to protect the environment and local population health (Lam et al., 2016, 2019). Physicochemical makeup presents enormous additional challenges to stabilize the landscape and prevent AMD tailing (Adiansyah et al., 2015; Santos et al., 2019), where the metal mobility in the soil varies with ionic strength, pH, type, and organic matter content (Ashworth and Alloway, 2007; Acosta et al., 2018). Although Chile currently has a robust regulatory system for tailings deposits, being able to become a national reference, it does not have the knowledge required for the remediation and rehabilitation of the sites that contain them. Since 2012, there is a law that regulates the closure of works and mining facilities, which requires a closure plan that includes measures and actions aimed at mitigating the effects derived from the development of the mining extractive industry, thereby ensuring their physical and chemical stability. Environmental problems associated with tailings disposal depends, among other factors, on the local climate. In the case of arid or semiarid climates, tailings are distributed to the environment through wind dispersion and erosion processes caused by water. While in the case of temperate climates, metal leaching and AMD formation have an impact on local currents (Mendez and Maier, 2008). Arid environments vary in terms of landforms, soils, fauna, flora, water balance, and human activities. The arid and semiarid regions are present in quite vast areas of the world; this is about a third to a quarter of the total landmass (Dan, 1973). Soils are often saline since evaporation rates are higher than rain and the presence of natural salts derived from saline rain, nondegraded minerals, and fossil salts (Mendez and Maier, 2008). Arid places present low content of organic matter and humidity and usually are subject to harsh environmental conditions, like radical temperatures and irradiation (Singh et al., 2009). In the Atacama Desert, in Chile, the arid climate is typified by frequent and warm winds with low rainfall. In arid and semiarid regions, the plant growth is constrained by several physicochemical factors that include extreme temperatures and high-speed winds. These factors involve the increase of extremely high salt concentrations, up to

118  Chapter 6 22 dS m−  1 because of elevated evaporation and reduced water penetration (Munshower, 1994; Padmavathiamma et al., 2014). Vegetation in arid areas is made up of ephemeral annual plants (growth limited to periodically short humid ones), succulent perennials (drought water plants), and nonsucculent perennials (suffer from arid environment stress) (Verheye, 2009; Padmavathiamma et al., 2014). In arid and semiarid environments, salinity and drought further increase the risks associated with the presence of pollutants (Padmavathiamma et al., 2014). Phytoremediation, a low-cost in situ technology, has arisen as the most favorable remediation technique for mine tailings with multielement contamination through the introduction of tolerant plants (Padmavathiamma and Li, 2007; Wang et al., 2017; Acosta et al., 2018; Santos et al., 2019). These set of technologies using plants to clean contaminated sites, has a minimal negative impact on the environment when treating mine tailings (Mendez and Maier, 2008), reducing the dispersion and bioavailability of metals, and returning the substrate to an acceptable ecological condition (Orchard et al., 2009). However, there are unfortunate cases of exotic plant species being introduced, having a rapid spread damaging native ecosystems (Ewel and Putz, 2004). Therefore, it is recommended to use native or endemic plants, already tailored to metallogenic, geographical, and climatic conditions of the area, giving added value to phytoremediation plans (Orchard et al., 2009). Phytostabilization of mining tailings is a natural alternative that improves the physical and chemical properties of the substrate, due to a vegetation cover, which makes the landscape esthetically pleasing, reducing the mobility of pollutants to other areas that can affect the affected populations. Also allows us to eliminate or reduce the toxicity of substances that may be harmful to human health and the environment. Phytoremediation has been investigated for decades, as a sustainable and environmentally friendly technique, also used for contaminants in soil, water, and sediment remediation. This technology uses the capability of some plants to accumulate, absorb, metabolize, stabilize, or volatilize pollutants present in the air, soil, sediments, or water (Hughes et al., 1997; Padmavathiamma and Li, 2007; Acosta et al., 2018). Its results depend on the natural mitigation by biodegradation and physicochemical mechanisms, which decrease the concentration of the contaminant (Padmavathiamma et al., 2014). Some species are considered heavy metal hyperaccumulators (collect very high metals concentrations in any aboveground tissue in their natural environment (Baker and Brooks, 1989)), although most of them have high water requirements for their development (Chaney et al., 1997). In the specific case of phytotechnologies applied to tailings, only species with the capacity to stabilize, extract and/or volatilize heavy metals have been identified, promoting phytostabilization, phytoextraction (Mendez and Maier, 2008) and, in a few cases, phytovolatilization (Singh et al., 2003; Moreno et al., 2004; Padmavathiamma and Li, 2007; Brooks, 1994; Lam et al., 2019).

Mine tailings phytoremediation in arid and semiarid environments  119 Mine tailings remediation is expensive compared with traditional technologies like chemical stabilization, excavation, and capping (Berti and Cunningham, 2000). Prices for pond tailings cover fluctuates subject to the functional requirements and site-specific factors (Sarkkinen et al., 2019). According to Sarkkinen et al. (2019), prices for pond tailings cover systems vary from 14.88 to 26.78€ m−  2 for their case study. However, every mine site is unique, and access to transportation, raw materials, labor, and material prices can vary greatly. For the case of phytoremediation, the remedial effects take longer than for traditional methods, which may restrict the use in some instances (Wolfe and Bjornstad, 2002; Mendez and Maier, 2008). Mine tailing’s physicochemical properties are inhospitable for plants and soil organisms. However, vegetation formation requires a soil system that can meet the nutrient and water needs of plants and associated organisms. Underdeveloped soils in mining ponds often require changes to improve fertility levels and support vigorous planting. Aided phytostabilization applied amendments to soil rehabilitation to cope with this weakness assisting phytostabilization, improving soil pH, salinity, and organic matter concentration (Zanuzzi et al., 2009). Techniques for remediation metal contaminated soils are expensive and environmentally invasive, where phytoremediation, a stable vegetable cover, is a long-term remediation option (Acosta et al., 2018). For in situ phytotechnologies, phytostabilization is the most proper for the restoration of mine waste and soils with multielement contamination, even in arid and semiarid climates (Santos et al., 2019). In situ remediation technologies immobilize heavy metals using chemical additives to remediate agricultural soil and alleviate environmental and health risks (Lim et al., 2013). The metal bioavailability decrease is obtained by the absorption with the humic substance on solid surfaces and complexation, depending on the type of soil, metal, degree of organic matter humidification, mineral, and salt content, and soil redox potential and pH effects of organic matter (Acosta et al., 2018). As indicated earlier, Chile is the largest copper producer in the world, where the Antofagasta region, located in the northern part of Chile, contributes over 50% of this valuable metal nationwide. The Atacama Desert in the Antofagasta region is considered the driest desert in the world (Romero et al., 2012; Collado et al., 2013). Some research has been carried out on plants adapted to these arid conditions, with different potential to stabilize metals in the rhizosphere area or to absorb and store metals in their tissues, which could be used in contaminated areas to reduce the mobility of toxic substances to other sites or other media (water and air). This is essential because the limiting factor for the production of plant biomass in arid and semiarid environments is water, this together with intrinsic abiotic stress, requires specific considerations, facilitating the process of phyto-strategies the use of endemic or native species that in addition to reducing the mobility of metals, can tolerate the natural water conditions of the area, since it must be considered that the phytoremediation system must be sustainable over time.

120  Chapter 6 The objective of this chapter is to offer the reader the results obtained through teamwork with native or endemic plant species on mine tailings located in the Antofagasta region. The species under study were Adesmia atacamensis (Lam et al., 2018b), Atriplex nummularia, Prosopis tamarugo, Schinus molle (Lam et al., 2017), Gazania rigens, and Pelargonium hortorum (Lam et al., 2018a).

6.2  Impact of past mining activity in Chile: Tailings In the operation phase, the mining project will generate value, provide essential metals for modern life, and contribute to local and national development. However, this stage has a limited life, depending on the useful lifespan of the mining project, because of the natural and gradual depletion of the natural resources present in the deposit (Lagos et al., 2018). Since the mineral of interest represents a small portion of the mined deposit, the process creates a large amount of waste, making a large volume of mine tailings and massive mining waste overall. Mine tailings have a wide variety of heavy metals and diverse concentration levels. Mine tailings storage facilities disable large hectares of soils for the agricultural sector and generate highly polluted soils whose elements will be mobilized based on the substrate physicochemical properties, as well as the climatic environments of the zone in which the deposit is situated (Mendez and Maier, 2008; Wang et al., 2017). The studies presented in this chapter were made with mine tailings from Chilean copper mining company Zaldívar (CMZ). CMZ mineral process consists of the following: first, the ore is extracted from the mine and transferred to the crushing plant, where it is reduced in size in a three-stage comminution circuit (primary, secondary, and tertiary crushing). It is subsequently agglomerated and leached in two stages in a dynamic stack. The impregnated rich leaching solution is processed by solvents and two electro-obtaining circuits at the SX-EW Plant, from which copper cathodes are obtained. An inheritance of mining is the phenomenon of AMD or acid rocks drainage, as a consequence of the oxidation of some mineral sulfides (pyrite, chalcopyrite, galena, among others) upon contact with water, and oxygen (obtain from the air), which can even be accelerated by the catalytic effect of certain bacteria that oxidize metal sulfides (Olsen, 2015; Pierre Louis et al., 2015; Cruz-Hernández et al., 2016). AMD is thought to be one of the primary water pollutants in many countries with a mining history (Nieto et al., 2013; Simate and Ndlovu, 2014; Dabrowski et al., 2015; Santisteban et al., 2015; Madzin et al., 2016). Although sulfides are very insoluble and stable for the subsoil reducing conditions, under certain atmospheric conditions, destabilization is caused due to oxidation reactions. AMD can lead to ecological damage and produce significant and permanent physicochemical alterations on ecosystems (Olsen, 2015). One of the most severe effects of AMD is water pollution, lowering its pH and introducing high concentrations of sulfates and heavy metals,

Mine tailings phytoremediation in arid and semiarid environments  121 affecting the ecosystems that inhabit it and generating problems associated with bioaccumulation and biomagnification, even seriously affecting the river fauna and create the loss of water resources (Clark and Lesser, 2013; Neuman et al., 2014; Simate and Ndlovu, 2014). According to a recent cadaster of April 2019 (SERNAGEOMIN, 2019) in Chile, there are 742 tailings deposits; listed as active, 14.0%; nonactive, 62.4%; abandoned, 23.2%; and in construction, 1.4%. In Chile several incidents of environmental impact had occurred on the marine ecosystem due to mining tailings deposits, impeding port activities, generating coast geomorphological modifications, and affecting recreational activities and coastal marine ecosystems (Castilla and Nealler, 1978; Castilla, 1983). The Coquimbo region, Chile, concentrates more than 50% of the deposits containing mine tailings; this region is one of the wealthiest producers of Au, Hg, and Cu in the Country, and some places have been mined uninterruptedly since the 16th century (Higueras et al., 2004), many of them are located with the inhabitants of this place for years, as it is shown in Fig. 6.1. Additionally, SERNAGEOMIN (2019) establishes that 639 are abandoned or paralyzed mining operations throughout the country, which constitutes significant sources of water, air, and soil contamination, as well as potential incidents that have caused severe damage to the environment and population health. SERNAGEOMIN proposes three phases to identify whether they correspond, according to the definition in Chile of a MEL, which is related to if they represent a significant and imminent risk. The first phase focuses on identifying,

Fig. 6.1 Tailings coexist with the Andacollo population.

122  Chapter 6 locating, and characterizing abandoned or paralyzed mining operations (their facilities) and their surroundings. The second phase contemplates the risk assessment and classification of the MELs. The third phase allows elaborating a ranking of the MELs, making a prioritization according to risks ordered from highest to lowest, so that in the future measures are implemented intended to mitigate or, at best cases, to reduce to zero the “significant risks” associated with MEL. Regarding SERNAGEOMIN records (2019), there are 8860 mining facilities in Chile, covering rocks and industrial minerals (clays, diatomite, carbonates, boron compounds, ulexite, phosphoric rocks, brines, caliche, sulfur, sodium compounds, ornamental rocks, siliceous, gypsum, pumice, pyrophyllite, zeolites, and peat); metallic mineral resources (copper, gold, iron, molybdenum, manganese, silver, zinc), and energy resources (coal, natural gas, oil), which constitute potential sources of MEL. The State of Chile must resolve the higher environmental costs caused by mining that have been transformed into debt for current and future generations. These companies, once the possibilities of extracting ore were exhausted, made the closure of mines, with low technological levels, without an adequate plan to guarantee the people health, security, and the environment; causing social, economic, environmental, and financial costs, that affect communities near sites where mining operations exist or have existed, or where the processes related with the extraction and processing of minerals are carried out, including power generation, mineral transportation, waste disposal, and others (Yurisch Toledo, 2016). Based on the previously mentioned factors, considering the adverse environmental repercussions generated by the presence of MEL distributed throughout the country, of which many of them are in total abandonment, without an owner taking responsibility, spontaneously, the following questions arise: Who takes care of them? Is the State of Chile responsible for ensuring the quality of life of all citizens? Unfortunately, to face these adversities, it is necessary to know which are the sites with potential contamination. To what degree and what is the variability of pollutants that compose it. What are the possible “victims” of these liabilities, and if there are resources, both economic and technological, to face this new obstacle produced by mining companies without a sustainable development vision, increasing overexploitation and resource deterioration, applying inadequate technologies lousy, and management practices? An answer to these MELs is required as soon as possible, which has generated unceasing problems for the population, exposing future generations. Great efforts are made to develop and apply technologies for the removal of polluting substances as well as for the recovery of metals of interest, such as the critical raw materials identified by the European Union (EU Commission, 2014).

Mine tailings phytoremediation in arid and semiarid environments  123

6.3  Mine tailings phytoremediation of in arid and semiarid environments Phytoremediation employs the physiological responses of plants to stress, which develops a series of defenses to deal with the harmful elements and the biological activities of soil microorganisms. These biochemical processes can occur outside or inside the plant system, depending on the mechanism by which the neutralization of the contaminant is carried out. Since other techniques for remediation of metal in contaminated soils are expensive and environmentally invasive, phytoremediation, a stable vegetable cover, is a long-term remediation option (Acosta et al., 2018). Phytoremediation can reestablish equilibrium in a stressed ecosystem through the natural, synergistic relationships between plants, microorganisms, and the environment. Therefore, phytoremediation includes various processes that occur in varying levels for different conditions, media, contaminants, and plants (Padmavathiamma and Li, 2007). Humans must be involved locally to build a suitable plant microbes’ community. Proper agronomic procedures, i.e., tillage and fertilizer, have also been used to improve natural degradation or containment processes (Cunningham and Ow, 1996). Broad studies on the phytoremediation suitability for organic and inorganic contaminants in soil and water have been carried out in recent decades (Singer et al., 2003; Pilon-Smits, 2005; Padmavathiamma and Li, 2007; Campos et al., 2008; Lee, 2013). Several plants, including rapeseed (Brassica napus L.), oats (Avena sativa), and barley (Hordeum vulgare), tolerate and accumulate metals, e.g., Se, Cu, Cd, and Zn (Ebbs and Kochian, 1997; McIntyre, 2003; Prasad and De Oliveira Freitas, 2003; Alkorta et al., 2004; Reisinger et al., 2008). The pollutants pass by apoplastic or sympathetic paths into the epidermis and via the Casparian strip into the endoderm, where they can be sorbed, bound, or metabolized. Endodermis metabolites reach the xylem and then are transferred in the transpiration stream. These compounds may be attached in plant tissue, metabolized, or released through the stoma pores into the atmosphere (Shimp et al., 1993; Paterson et al., 1994). Reboredo (2001) detected that carbohydrates and proteins of cell walls were favored binding sites of Zn in the halophyte Halimione portulacoides. There is no confirmation that plant roots can absorb water-insoluble oil and oil derivatives. Henceforward, it should be assumed that phytoremediation for oily soils makes use of microbial activities within the rhizosphere soil rather than those of the plant itself. In general, inorganic components easily absorbed by plants include As, Cd, Cu, Ni, Se, and Zn; moderately bioavailable metals are Co, Fe, and Mn, while Cr, Pb, and U have very low bioavailability. Notwithstanding, it should be considered that some of the considered environmental pollutants at specific concentrations are also essential nutrients for plants (ITRC, 2009).

124  Chapter 6 In a phytoremediation process, by contacting the plant with a substrate containing a high variability of metals and metalloids at high concentrations, such as tailings, an additional source of stress is being provided for plant species (Luo et al., 2017), also considering the conditions typical of arid and semiarid environments (thermal stress due to heat, wind force, low or no rainfall, among others). Phytoremediation requires the use of endemic or native species, which have adapted the systems to extreme conditions, as well as the ability to stabilize or extract and accumulate the metals and metalloids present in the substratum. Phytoremediation entails the plants’ growth and has chemical and biological impacts on the soil in arid environments. The soil clods parting is a physical effect of the tips of the roots that push through the soil as they grow. Root growth can form macropores in the soil, contributing to soil aeration, water retention capacity, and contaminants transport in the soil (Luo et al., 2017). The rise in soil organic matter content due to the plants’ growth enhances the structure and “workability” in arid soils. Root exudates organic acids, phenolics, sugars, polysaccharides, among others, can change the metal speciation, absorption of metal ions, and the simultaneous release of protons, which acidifies the soil and promotes the transport of metals and bioavailability (Ernst, 1996; Montiel-Rozas et al., 2016). Phytostabilization immobilizes metals and metalloids by its accumulation in roots or precipitation in the rhizosphere, reducing the bioavailability of pollutants, increasing organic matter content, improving physical properties, reducing wind and water erosion, and increasing biodiversity (Acosta et al., 2018). The metal bioavailability reduction is due to the absorption on solid surfaces and complexation with humic substance, depending on the metal, type of soil, degree of organic matter humidification, metal and salt content, and effects of organic matter on soil redox potential and pH (Acosta et al., 2018). In some cases, the altered metal specification can lead to enhanced metal precipitation and immobility, thereby decreasing environmental impact (Padmavathiamma and Li, 2008). The organic elements in the root exudates can promote microbial growth in the rhizosphere. The mycorrhizae related to some plant roots can also impact the soil microclimate, supporting phytoremediation. The soil organic matter content assisted by decaying root and plant remains modified by the pedogenic properties thereby directing to humification and improved sorption of contaminants (Ernst, 1996). Mine tailings physicochemical characteristics are negative to natural plant growth, e.g., elevated pH, salinity, heavy metal concentration, and deficit in water retention capacity, soil organic matter, and fertility of the soil (Wang et al., 2017). It is important to highlight that pH values in some tailing ponds are acidic, even sometimes the values observed are lower than 3; and, these values affect the heavy metal mobility, generating important environmental risks (Martínez-Martínez et al., 2019). Various phytostrategies can lead to degradation of contaminants, elimination (by accumulation or dissipation), or immobilization. Care must be taken to ensure that no phytoremediation strategy involves the unnecessary transport

Mine tailings phytoremediation in arid and semiarid environments  125 of contaminants to other media. The later applies to all pollutants such as petroleum hydrocarbons, chlorinated solvents, metals, radionuclides, nutrients, pentachlorophenol (PCP), and polycyclic aromatic hydrocarbons (PAHs). Also, plants play an unintended part in the phytoremediation of oily soils by promoting microflora in the rhizosphere (Radwan et al., 2005; Singh et al., 2009). For phytoremediation, direct sowing and the use of transplants are recommended. To sow the seeds directly into polluted soil results in inconstant plant growth contrasted to seedling transplantation. Therefore, the use of transplants provides better results, although they require more labor (Mendez and Maier, 2008). Fig. 6.2 shows how native species naturally grow and develop near the tailings located in Andacollo, sites impacted by mining operations, additionally to the fact that the climate of Andacollo is desertic, which demonstrates the potential to evaluate phytotechnologies, regardless of the type of weather. Two main types of phytoremediation have been considered for use in the treatment of mining tailings: phytoextraction and phytostabilization. In the case of arid or semiarid regions, the plants used must be tolerant of drought and salinity to withstand the adverse conditions of the site where the tailings are located (Mendez and Maier, 2008).

Fig. 6.2 Vegetable species adapt to the extreme conditions of the mining sector. Photos are taken in the vicinity of tailings in Andacollo, Chile.

126  Chapter 6 Mine tailings phytostabilization in arid or semiarid climates requires the use of drought, salinity, and high metal tolerant plants (Mendez and Maier, 2008). Phytostabilization uses plants to immobilize contaminants in the substrate, preventing their migration, and reducing metals availability. It is more effective in fine-textured soils with a high concentration of organic matter. Besides, the low concentration of metals in aerial tissues eliminates the need to treat the crop as hazardous waste (Padmavathiamma and Li, 2007; Orchard et al., 2009). Phytostabilization presents specific difficulties, such as since pollutants stay in place, vegetation and soil may require maintenance for a long time while in the root zone, root exudates, pollutants, and soil amendments should be examined to avoid a rise in solubility and leachate. Phytoextraction involves crops of tolerant and hyperaccumulating plants of metals, whose purpose is to reduce the substrate concentration. The effectiveness of phytoextraction is dependent, among other factors, on the availability of metals to be absorbed by plants (Padmavathiamma and Li, 2007; Mendez and Maier, 2008). With some metals, the value of recovered metal could provide further motivation for phytoremediation. Consequently, if phytoextraction could be combined with biomass generation and as a source of energy, with the residual ashes available to be used as a mineral, then it could be transformed into a profitable operation (Padmavathiamma and Li, 2007). Phytoextraction of mine tailings metals faces multiple significant challenges. First, hyperaccumulation is generally bad due to the low bioavailability of metals in tailings amended, e.g., with compost, to sustain plant growth. Also, these substrates are polymetallic, which could encompass multiple species of plants and ecotypes for metal removal, because many hyperaccumulators can only accumulate one or two metals (Mendez and Maier, 2008). On the other hand, metal chelation has been proven to overcome phytoextraction inefficiency. However, the use of chelates to increase the absorption of metals may result in phytotoxicity to plants. The second problem is that the solubility of metals increases after the application of the chelate, which can cause leaching of the metal and possible pollution of groundwater (Mendez and Maier, 2008). Additionally, the chelates addition effects to the microbial community are usually neglected. It was reported that several synthetic chelates that can stimulate phytoextraction could form chemically and microbiologically stable complexes with heavy metals, threatening soil quality, and groundwater contamination (Padmavathiamma and Li, 2007). Due to the potentially toxic levels of metals that can be accumulated in the plant aerial part, the access to the system must be controlled and then removed plant biomass must be stored or disposed of properly. Therefore, recycling or reuse of collected metals is ideal, corresponding to phytomining (Padmavathiamma and Li, 2007; Mendez and Maier, 2008). Phytomining is the elimination of mineral metals in situ from subeconomic bodies or polluted mining sites,

Mine tailings phytoremediation in arid and semiarid environments  127 intending to recover commercial quantities from plants. Wherein, the dry material decreases to ashes, with or without energy recovery, when processed by other methods and allows metals in ash or ore to recover by conventional methods of metal refinery like acid dissolution and electro-obtaining (Sheoran et al., 2009). In general, in arid environments, the addition of organic and inorganic amendments and irrigation contributes to increasing successful coverage of the site. Organic amendments reduce metals bioavailability, and irrigation increases the plant establishment. Additionally, the use of transplants could guarantee high odds of the establishment of the transplanted species (Mendez and Maier, 2008). Studies strengthen the notion that the amount, and type of amendment needed are reliant on the plant’s growth needs and the physicochemical properties of the tailings themselves. Therefore, the amendment conditions are specific to the site and plant species (Mendez and Maier, 2008). Additionally, it should be considered that amendments stabilize pollutants, and plants use could contribute to phytostabilization by reducing water quantity moving through the soil and by physical stabilization of the soil against erosion. Some examples of amendments applied to aid the phytostabilization process are fly ash, phosphate-based materials, biosolids, compost, litter, and animal manure (Santibañez et al., 2012; Wang et al., 2017), sludge (Asensio et al., 2013; Lim et al., 2013; Wang et al., 2017), liming materials (Gadepalle et al., 2007; Parra et al., 2016; Pardo et al., 2017; Clemente et al., 2019), eggshells (Ok et al., 2011; Ahmad et al., 2012a; Lam et al., 2016), waste oyster shells (Ok et al., 2010), cow bones (Ahmad et al., 2012c), mussel shells (Ahmad et al., 2012b,c), natural zeolite (Shi et al., 2009), poultry waste materials (Hashimoto et al., 2008), and biochar (Fellet et al., 2011; Moreno-Barriga et al., 2017a,b,c; Wang et al., 2017; Álvarez-Rogel et al., 2018; Abbaspour et al., 2020). Further information can be found in Section 6.5.

6.4  Endemic and native species in mining areas in arid and semiarid environments Autochthones plants are used in environmental rehabilitation programs due to their well suited to multiple stress factors relating to mining areas and climate conditions (Santos et al., 2019). Several studies have been carried out on species of this genus, namely, A. coquimbana, A. atacamensis (Lam et al., 2018b), A. deserticota, A. halimus (Clemente et al., 2012; Acosta et al., 2018), A. repanda, A. semibaccata, and A. nummularia (El-Shatnawi and Abdullah, 2003; Lam et al., 2017). They also have mechanisms that enable them to develop in soils with high concentrations of sodium, so that they adapt without any problems in the soils of arid and semiarid environmental conditions (Meneses and Squella, 1996). A. halimus is broadly used for phytostabilization purposes in contaminated sites, it may absorb and translocate high metals concentrations to the airborne tissues in

128  Chapter 6 saline contaminated sites (Acosta et al., 2018). In Spain, A. halimus L. was used for phytoremediation experimentation in a semiarid region heavily polluted by trace elements of Pb, As, Cu, Cd, Mn, and Zn aided by compost and pig slurry on soil amendment (Clemente et al., 2012). The results show the possibilities of A. halimus, coupled with an organic amendment, for phytostabilization in arid and semiarid areas (Clemente et al., 2012). A. halimus showed phytotoxic concentrations of Zn in their leaves by Martínez-Martínez et al. (2019), suggesting to avoided these species in soils contaminated with large concentrations of Zn. However, in this study, Lygeum spartum and Piptatherum miliaceum were effective in the phytostabilization of Pb, Zn, and As because they accumulate large concentrations of metals in their roots, with little aerial translocation (Martínez-Martínez et al., 2019). Regarding the crops used in phytoremediation projects, the information on yields or nutritional requirements is limited, with some exceptions, such as Brassica juncea (Indian mustard) and Helianthus annuus (sunflower) (Hoffmann et al., 2004). There are studies carried out by different international institutions that provide relevant information on plant species that can potentially be used in phytoremediation, e.g., genus Atriplex (El-Shatnawi and Abdullah, 2003). Silybum marianum and Piptatherum miliaceum were cultivated in a greenhouse with inorganic and organic amendments to restore trace element contaminated soil (Clemente et al., 2019). These plants were selected due to their elevated biomass production and tolerance to a high concentration of trace elements in soil and growth under Mediterranean weather conditions (Clemente et al., 2019). P. miliaceum was applied to pyritic mine tailings for improved metal immobilization, enlarged microbial communities, and increased soil structure (Moreno-Barriga et al., 2017c). Twelve wild plant species suitable for the mine tailings remediation in arid environments can grow in mine tailings, accumulate concentrations of potentially toxic elements mentioned previously generally accepted phytotoxicity levels, and are fit to form a vegetation cover in sterile mine tailings in the Zimapan region, Mexico (Sánchez-López et al., 2015a,b). As examples: Dalea bicolor, Viguiera dentata, Brickellia veronicifolia, Dichondra argentea, Cuphea lanceolata, Ruta graveolens L., Pteridium sp., Juniperus sp., Aster gymnocephalus, Crotalaria pumila, Gnaphalium sp., and Flaveria trinervia (Sánchez-López et al., 2015a,b). These plants have possible use in phytoremediation, based upon potentially toxic elements concentration in the roots and outbreaks, bioconcentration and translocation factors. From the results, Pteridium sp. is appropriate for Cd and Zn phytostabilization. Gnaphalium sp. is a possible phytoextractor for Cu and Crotalaria pumila for Zn, and Aster gymnocephalus for Cd, Cu, Pb, and Zn (Sánchez-López et al., 2015b). Lolium perenne and Polypogon australis were used to phytostabilize copper mine tailings under semiarid environment to promote cohesive waste management processes, locally, and restore large-scale postoperative tailings storage facilities (Santibañez et al., 2012).

Mine tailings phytoremediation in arid and semiarid environments  129 All treatments under study improved the chemical and microbiological attributes of waste and resulted in a substantial rise in plant yield after 3 years (Santibañez et al., 2012). Hyparrhenia hirta, Zygophyllum fabago, and Bellota hirsute species that have naturally populated some parts of the tailing in Spain. Zygophyllum fabago is a perennial plant species, resistant to drought, and presents tolerance to high concentrations of Cd (Kabas et al., 2014). Zygophyllum fabago accumulates 750 mg kg−  1 of Zn in shoots. Hyparrhenia hirta accumulates around 150 mg kg−  1 Pb in shoots and roots (Conesa et al., 2007). Bellota hirsute has the capacity of bioaccumulation As, Cr, Cu, Fe, and Pd, transferring a substantial concentration of them to comestible parts without surpassing the toxic limits for animals, or its capacity of colonization and development (Gabarrón et al., 2018). Some other examples are Alyssoides utriculata, Atriplex halimus, Cistus libanotis, Dittrichia viscosa, Hirschfeldia incana, and Pinus halepensis, are specific to Mediterranean regions and have been informed to be appropriate for phytostabilization of mining sites in semiarid climates (Auguy et al., 2013; Párraga-Aguado et al., 2013; Roccotiello et al., 2015; Doumas et al., 2018). A past uranium mill in Arizona was phytoremediated by setting and irrigating deep-rooted native shrubs Sarcobatus vermiculatus and Atriplex canescens. The phytoremediation is a viable alternative to pump, and treatment solutions in arid and semiarid areas (Jordan et al., 2008).

6.5  The effect of the amendment on tailing availability Mine tailings harm local land resources and generate several environmental contaminations, posing a risk to human health due to their loose nature and easy flow and collapse when stacked. Mine tailing remediation methods aim to enhance the ecosystem of mining areas and maximize the use of tailing resources by chemical remediation, bioremediation, and physical treatment (Wang et al., 2017). Mine tailings phytoremediation benefits soil stabilization without damaging topsoil, maintains or improves soil utility and fertility, enhances organic matter, biological activity, and nutrient concentration, also generates biomass or biofuel production, and carbon sequestration (Wang et al., 2017). Stable soil structure is essential to maintain the agricultural productivity and reduce erosion, not presented by the physicochemical properties of mine tailings alone. Therefore, adequate amendments must be applied to enhance mine tailings’ biological, chemical, and physical properties and enhance plant establishment (Santibañez et al., 2012; Wang et al., 2017). The concentration of soluble and extractable trace element has been used to evaluate the amendments efficacy and plant performances in the restoration process (Moreno-Jiménez et al., 2009; Lopareva-Pohu et al., 2011; Alvarenga et al., 2018; Clemente et al., 2019).

130  Chapter 6 Excessive heavy metals in plants often inhibit root growth and result in leaf chlorosis and lower biomass production (Jadia and Fulekar, 2009; Wang et al., 2017). Therefore, amendments application is required since it improves substrate physicochemical properties for plants and soil microbiota growth, immobilizing pollutants by several chemical processes (Lim et al., 2013; Santos et al., 2019). Amendments and conditioners used in remediation processes by-products and waste materials from different agrochemical processes present interesting environmentally sound options for their management, reuse, and recycling (Clemente et al., 2019). Some examples are fly ash, lime, phosphate-based materials, biosolids, compost, litter, and manure (Santibañez et al., 2012; Wang et al., 2017). Sludge amendments neutralize pH, reduce metal concentration, and increase soil fertility, improving biological properties and soil biological community structure (Asensio et al., 2013; Lim et al., 2013; Wang et al., 2017). Liming materials have been used in acidic trace element contaminated soil with animal manure to increase soil pH, allow plant survival, and immobilize pollutants (Gadepalle et al., 2007; Parra et al., 2016; Pardo et al., 2017; Clemente et al., 2019). Natural additives found in waste materials such as waste eggshells (Ok et al., 2011; Ahmad et al., 2012a; Lam et al., 2016) waste oyster shells (Ok et al., 2010), cow bones (Ahmad et al., 2012c), mussel shells (Ahmad et al., 2012b,c), natural zeolite (Shi et al., 2009), and poultry waste materials (Hashimoto et al., 2008) have been investigated and have immobilizing heavy metals in contaminated soil (Lim et al., 2013). Additionally, biochar has been applied to mine tailings and contaminated soil for phytostabilization (Fellet et al., 2011; Moreno-Barriga et al., 2017a,b,c; Wang et al., 2017; Álvarez-Rogel et al., 2018; Abbaspour et al., 2020). Acosta et al. (2018) reclaim tailing pond by prompting native species growth through natural colonization using amendments of marble waste, pig slurry, and a combination of them. The marble waste contains calcium carbonate and helps to neutralize the acidity, immobilize metals, and improve soil degradation (Acosta et al., 2018). Various studies have pointed out that soluble organic wastes are successful in improving the solubility of heavy metals (Ashworth and Alloway, 2007; Abbaspour et al., 2008; Antoniadis et al., 2017; Acosta et al., 2018). The oxidative stress measured by Clemente et al. (2019) validate the combination of organic (pig slurry) and inorganic (paper mill sludge or commercial red mud derivate) amendments suitability, for the phytostabilization of contaminated soil with trace elements. Although the combination of inorganic and organic soil amendments allows the survival and appropriate growth of native plant species in highly polluted soil with trace elements (Clemente et al., 2019), when applied, isolated organic materials, compared with inorganic components, buffer soil pH, affects adsorption and complexation of metals thereby improving soil properties, water retention capacity, water infiltration, and nutritional status (Wang et al., 2017). Also, the inorganic amendment was the least efficient in removing salts (Lam et al., 2016).

Mine tailings phytoremediation in arid and semiarid environments  131 An alkaline barrier stabilizes sulfide-rich wastes by reducing oxidation and capillary rise of acid solutions, rich in metals and metalloids, and in combination with Technosols proven to be efficient and sustainable in the long-term (Santos et al., 2019). The movement of metals in the soil varies according to pH, ionic strength, type, and amount of organic matter (Ashworth and Alloway, 2007). The rhizosphere rises soil pH when parts absorb nitrates and other anions in more amounts than cations, therefore, roots release bicarbonate to maintain electrical neutrality, increasing soil pH (Acosta et al., 2018). Some microorganisms are useful in phytoremediation by modifying their soil environment, reducing heavy metal toxicity, increasing heavy metal bioavailability, and biomass production, e.g., plant growth-promoting bacteria, filamentous fungi, and biodegradative bacteria (Cao and Liu, 2015; Wang et al., 2017). In general, plant roots excrete into the rhizosphere some organic and inorganic compounds, a mix of sugars, organic acids, vitamins, and ions, increasing the microbial activity (Acosta et al., 2018). The microorganism can reduce certain kinds of organic acid, improving heavy metal solubility by modifying their soil environment, including oxidation-reduction potential and pH. The polysaccharides secreted by microorganisms can bind soil particles reducing erosion, therefore, enhancing soil structural stability and improving soil aggregates structure (Wang et al., 2017). The presence of arbuscular mycorrhizal fungi (AMF) contributes to plant growth and nutrient acquisition, by the development of different mechanisms that encourage plants to grow in habitats polluted with heavy metals with highly toxic concentrations (Khan, 2005; Meier et al., 2012). AMF provides a system for symbiotic interaction between the hyphal networks functionally extending up to the root system of their plant hosts. This symbiosis with AMF and host plant has the potential to take up heavy metals from a broadened substratum (Göhre and Paszkowski, 2006), performing an important part in metal tolerance and accumulation. This association could contribute to the metals immobilization in the substrate, to the increased absorption and consequent accumulation of metals in the aerial tissues of plant species (Gaur and Adholeya, 2004). Plant growth-promoting bacteria facilitate plant growth by raising their tolerance to acidic pH and metals, reduce the amount of compost required in amendments, expand metal accumulation through the release of organic acids, siderophores, and biosurfactants (Wang et al., 2017). Rhizobacteria increase phytoremediation efficiency by increasing biomass production and alter metals bioavailability in mine tailings (Wang et al., 2017). Fungi, compared to bacteria, present higher tolerance for extreme climate, pH, heavy metals, and nutrients (Wang et al., 2017). Aspergillus niger, Rhizopus arrhizus, and Mucor rouxxii are filamentous fungi that can adsorb metal ions like Cu2  +, Co2  +, Pb2  +, Zn2  +, and Cd2  +, and can be used as sorbent. Microorganisms like S. barnesii, Sulfurospirillum arsenophillum, Chysiogenes arsenatis, and Bacillus arsenicoselenatis have a large capacity for mobilizing As and reducing as As (V) (Wang et al., 2017).

132  Chapter 6 The microbiological activity of the soil is of significance for the development of the plants because the soil microorganisms release nutrients from the mineral or organic reserves with enough speed to allow their growth. Without the recycling processes carried out in the soil, elements such as nitrogen, phosphorus, potassium, and several other nutrients would accumulate in inert masses without being used by vegetation. Mining is responsible for major environmental damage, like air contamination by particulate matter, toxic air emissions, and depletion and pollution of surface and groundwater resources (Lam et al., 2016). Mine activity results in shifts in the landscape, destruction of habitats, soil and water pollution, degradation of land resources, generation of AMD, erosion, and sedimentation processes, liberation metals, and metalloids, among others (Acosta et al., 2018). Tailings in Chile, historically, were left without adequate management due to inadequate legislation. Currently, the law entails that tailings should be physically and chemically stabilized (Lam et al., 2016, 2019). Mining companies are obligated to possess a closure plan that ensures the stability of tailings landfills to protect the neighboring environment and health of the local population (Lam et al., 2016). Lam et al. (2016) assessed the heavy metal mobility of copper mine wastes classified as saline sodic, high concentration of metals (especially Fe, Al, and Cu), and pH 8.4. The physicochemical properties of the earth and surrounding soil, and the effects of two changes (CaCO3 and organic matter) have been investigated. The tailings can still contain large concentrations of sulphide minerals, which may undergo oxidation, producing a major source of metal and acid contamination (Lam et al., 2016). Fig. 6.3 shows the tailings in which the authors’ investigations were carried out, presents superficial cracks, typical

Fig. 6.3 CMZ tailings present surface cracks typical of an arid environment.

Mine tailings phytoremediation in arid and semiarid environments  133 of an arid zone, we will call these tailings from now CMZ. The region where the project is located in one of the driest in the world and is characterized by high solar radiation and a high concentration of salt in the soil. The environmental conditions determine that hardly any vegetation is mainly concentrated in the fluves and generally in the interfluves. Biogeographically, this region is embedded in xeromorphic ecosystems, characterized by extreme drought (high daytime temperatures, large heat fluctuations, minimal, and cyclic rains), especially in the tropical ecoregion of the periaroid desert extended from the rocky coast to the Andean foothills 2500 m of height, including the desert plain an intermediate area. In this region, height and relief determine the presence of vegetation, been characterized by a short vegetation period, which defines a very specific plant physiognomy (Lam et al., 2018b). Lam and collaborators (2018a,b) identified and evaluated hyperaccumulator plant capacity on copper mine tailings, under arid conditions. Regarding the amendments, the tailings understudy on which calcium carbonate obtained from eggshells has been incorporated are shown in Fig. 6.4.

Fig. 6.4 CMZ tailings with added CaCO3 amendments obtained from eggshells.

134  Chapter 6 On the one hand, tailings have large quantities of metal(loid)s that might move into natural ecosystems and change the activities and functions of soil micro and macroorganisms. Microorganisms can adapt and resist metallic stress, and a few of them can improve plant habitat and the phytoremediation process. AMFs role in phytoremediation is to contribute to the production and growth of nutrients for plants (Meier et al., 2012). These fungi use several mechanisms to promote plants to grow in soils with high concentrations of toxic metals. It is essential to point out, AMF metal tolerance mechanisms, and their role in promoting phytoremediation processes, due to AMF propagates in contact with growing roots (Meier et al., 2012). Fig. 6.5 shows the incorporation of AMF in the backfill soil, and in Fig. 6.6, the AMF activated in A. nummularia is visualized (CMZ tailings). Poultry waste and ammonium nitrate were evaluated, to conditioning and stabilizing mine tailings, and to aid the vegetation cover settlement. The results of metal mobility and availability showed that the use of chicken bone ash (poultry waste) decreases the concentrations of soluble metals, specifically Fe and soluble Mn. On the other hand, the acidification produced by the nitrification of ammonium nitrate does not significantly increase the content of metals in the leachates. Therefore, the use of this for fertilization does not involve risks of phytotoxicity. The concentrations of macronutrients and trace elements are within the ranges suitable for plant nutrition; hence, the treatments are useful for both fertilization and phytoremediation. Santibañez et al. (2012) assessed the effectiveness of organic- and hard-rock mine waste type materials for the phytostabilization of copper mine tailings. Six amendments, namely,

Fig. 6.5 AMF incorporation in the backfill soil before the transplantation of the species (CMZ tailings).

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Fig. 6.6 Mycorrhizal fungi activated in the roots of A. nummularia (CMZ tailings).

waste-type locally available grape and olive residues, biosolids, goat manure, sediments from irrigation canals, and rubble from Cu-oxide lixiviation piles were evaluated (Santibañez et al., 2012). Results showed that biosolids and grape residues, alone or mixed, were the most appropriate organic amendments when added to tailings up to a depth of 20 cm. Rubble from Cu-oxide lixiviation piles and goat manure had effective results, improving tailings microbiological and chemical properties and significantly intensifying plant yield after 3 years (Santibañez et al., 2012). The phytostabilization allows the inmovolization of metals contained in the mine tailings into the substratum, through adsorption and accumulation into the roots or rhizosphere. The location where phytoremediation takes place needs regular monitoring to make sure that the optimal stabilizing conditions are achieved (Khalid et al., 2017). Inappropriate remediation monitoring is a cause of failure (Kuppusamy et al., 2017). Monitoring the soil after aided phytostabilization is necessary to assess the long term evolution of soil properties, the ecological succession, and the evolution of metal concentrations, allowing a better understanding of the ecotoxicological results (Martínez-Martínez et al., 2019). Microbial biomass and activity, greenhouse gas emissions, organic matter stability, and aggregation, monitoring should be developed to conclude that the addition of different organic and industrial materials to mine residues efficiently contributes to the formation of healthy soil with the presence of stable soil aggregates, soil organic matter and active microbial communities (Moreno-Barriga et al., 2017a,b). Chemical additives can be toxic in the soil and lead to risks of leaching of metals into groundwater, it might be of interest to couple the phytoremediation with monitoring of metal displacement in the

136  Chapter 6 soil, through a noninvasive control of water displacement (Khalid et al., 2017; Vocciante et al., 2019). The monitoring at the end of each cultivation phase can evaluate and verify the reclamation trend and duration of the pilot test, providing indications on the removal rate of contaminants and allowing an evaluation of the effectiveness of the technology (Vocciante et al., 2019). The implementation of suitable remediation strategies must be applied where the remediation technology is put into action along with long-term monitoring and maintenance. If risk persists, then the site must be subjected to further remediation (Kuppusamy et al., 2017).

6.6  Assessment of phytoremediation potential of mine tailings using (results of a case study) This section presents the results obtained from the evaluation of the metal accumulation capacity of six plant species, Atriplex nummularia, Prosopis tamarugo, Schinus mole, Gazania rigens, Pelargonium hortorum, and Adesmia atacamensis, in the CMZ tailings. In the area where CMZ tailings are located, the flora does not form homogeneous units of vegetation, only dispersed populations or communities. The most common species correspond to A. atacamensis, detected in 133 sites, where 116 forms populations and the remaining 5% are associated with communities of C. salsoloides, O. hypsophylla, S. philippianum, and E. breana. A. atacamensis and C. salsoloides were selected initially as study subjects considering the status and quantity of samples of the species. Additionally, the species P. tamarugo, S. molle, G. rigens, P. hortorum, and A. nummularia were evaluated because they develop in arid areas and saline environments. These last five species were transferred to the mining company, to study with the mine tailings and were conditioned in a nursery installed at the site for 45 days, as shown in Fig. 6.7. All species were subjected to daily irrigation of 200 mL of water. Subsequently, the species were transplanted into bags containing tailings and amendments. Organic compost, calcium carbonate, and AMF were tested as an amendment. The plants were left outdoors in the neighborhood where the tailings were studied for 15 days to acclimatize them to the extreme conditions of the site (temperature, winds, air pollution), as shown in Fig. 6.8. Then, after 15 days, the species were transplanted to the tailings, for which it was necessary to plow the tailings with a backhoe machine (see Fig. 6.9). Then, the holes with the required dimensions were made, depending on the type of species and incorporate the amendments in the required doses, using the Hirzel method (2010) for the case of the organic amendment

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Fig. 6.7 A. nummularia and P. tamarugo in conditioned nursery inside the CMZ tailings reservoir.

Fig. 6.8 Transplant of species to tailings conditioned and arranged outdoors, in the tailings area.

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Fig. 6.9 Plow with a backhoe in the tailings site.

and the Sobek method (1978) for CaCO3. The shovel was covered with a plastic bag to avoid external contamination. As can be seen in Fig. 6.10, the area was sized, demarcated with strings, and sized each hole. Once the holes were made, organic compost and CaCO3 were added at the dose determined by the Hirzel method (2010) and Sobek method (1978), respectively, the purpose of CaCO3 was not to increase the pH, but to discharge sulfate concentration and high electrical conductivity, the objective was to produce gypsum, a more harmless product. The area was watered until saturation for 42 days (see Fig. 6.4). Fig. 6.11 shows the irrigation of transplanted species in CMZ tailings. Fig. 6.12 shows the result of sowing alfalfa in the tailings, which developed very well. However, it was not considered in this investigation, given the high-water requirements for irrigation, a resource that is very scarce in the zone. Fig. 6.13: A. atacamensis in the process

Fig. 6.10 Sizing and tacking holes to perform the transplant in situ.

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Fig. 6.11 Drip irrigation of transplanted species in situ, in CMZ tailings.

Fig. 6.12 Alfalfa, which was planted in the CMZ tailings.

of phytoremediation CMZ tailings shows the photograph of the phytoremediation system applied to the CMZ tailings. To determine the ability to apply phytotechnologies to the CMZ tailings, in the species A. nummularia, P. tamarugo, and S. molle, values of elements of an environmental connotation for Chilean mining were measured: Cd, Cu, Mn, Fe, Pb, and Zn, using the following three treatments: tailings control without amendment (T0), tailings more CaCO3 + compost (T1), and tailings + CaCO3 + compost + AMF (T2). The AMF used was Glomus intraradices. In the case of G. rigens, P. hortorum, and A. atacamensis, values of the same elements were measured, using the following three treatments: tailings control without amendment (T0), take more 4% CaCO3 + 3% vermicompost (VC) + AMF (T1), and tailing +  8% CaCO3 + 6%

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Fig. 6.13 A. atacamensis in the process of phytoremediation CMZ tailings.

VC + AMF (T2). Besides, for treatments T1 and T2 (T0 is the control treatment, therefore, it does not involve the use of amendments), subsequent levels of AMF were: 0, 10, 15, and 20 g m−  2. The Baker and Brooks criteria (1989) and the BCF were used to assess species as hyperaccumulators. Next, the selection process of the six indicated plant species and the results obtained for each of them will be presented.

6.6.1  A. atacamensis The presence of the different plant species naturally present in four sites located in the Antofagasta region, close to each other, were evaluated, one of which corresponds to CMZ, the other three will be named with fantasy names GB, CME, and MLB, determining the presence of A. atacamensis and C. salsoloides in three of the four deposits (CMZ, GB, and CME), so it was first decided to select these two species to assess their potential for soil remediation of soils that have been exposed to copper mining. The four deposits extract copper, so it is considered that the metals present, plus soil conditions such as pH and electrical conductivity, height, in addition to the weather, are tolerated by these plants. Fig. 6.14 presents the photo showing the natural presence of A. atacamensis and C. salsoloides at the study site.

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Fig. 6.14 Natural presence of A. atacamensis and C. salsoloides at the CMZ study site.

It was observed that the specimens of both species were in different states dead, in precarious conditions, alive, and others in the process of flowering. In the case of A. atacamensis present in CMZ 103 dead specimens, 92 specimens in precarious conditions, 74 live specimens, and seven live specimens were found in the process of flowering. Regarding C. salsoloides, 29 dead specimens, five in precarious conditions, two live, and one specimen in the process of flowering were found near CMZ. Although the specimens of this species found in the CMZ deposit are only 37, this species is attractive to evaluate, since in one of the nearby deposits more than 4000 specimens were found, another essential characteristic is that at any time of the year, it is always possible to find specimens blooming. A vital factor to consider is the height, for instance, “GB” at the altitudes between 2000 and 2400 m above sea level (m.a.s.l), the presence of any specimen was not found, A. atacamensis or C. salsoloides; 385 and 205 specimens of C. salsoloides and A. atacamensis were found, between 2400 and 2600 m.a.s.l. About 2600 and 2800 m.a.s.l., were found 715 and 240 copies of C. salsoloides and A. atacamensis, respectively; between 2800 and 3000 m.a.s.l., 2610 and 506 copies of C. salsoloides and A. atacamensis were found, and finally, between 3000 and 3200 m.a.s.l., 300 and 248 copies of C. salsoloides and A. atacamensis were found; which indicates that the height 2800–3000 m.a.s.l., favors the development of both species. C. salsoloides could not be evaluated because in the period of experimentation only eight live specimens were found, five were in precarious conditions, therefore, it was impossible to use this species, besides, to not affect site biodiversity, it was decided not to extract specimens from the sector. The bioconcentration factor (BCF) and the translocation factor were determined to assess the potentials of all the species involved in a phytoremediation process. For example in the case of A. atacamensis, regarding BCF values, all were less than 1, which is undeniable, given the high concentration of metals in tailings, which is not comparable

142  Chapter 6 with values of soils contaminated by a specific activity, other than mining. However, BCF values for Cu range between 0.43 and 0.88, indicating that this endemic species is Cu hyperaccumulator; in the case of tailings without amendments, a value of BCF 0.46 was obtained, although it is less than the unit value, it is observed that the species can develop naturally, and is suitable for phytoextraction. The highest BCF values were obtained with the T2 treatment (tailings plus 4% CaCO3 + 3% VC) and AMF inoculation (20 g m−  2). Another metal that obtained a BCF value higher was Zn, whose values fluctuate between 0.01 and 0.31. It is also observed that the T2 treatment is the most appropriate, but the effect of AMF inoculation is not significant. According to the criteria given by Baker and Brooks (1989), A. atacamensis can be considered as a copper hyperaccumulator species, and, therefore, is suitable for phytoextraction. Regarding the translocation factor (TF) values, the highest values were obtained by Fe (1.41–3.94), Pb (1.67–4.60), and Zn (2.39–4.71). Therefore, these metals can be translocated from the roots to the aerial part. The results obtained indicate that the contribution of the amendments could improve the phytostabilization of these metals in the roots. Examples of A. atacamensis are shown in Fig. 6.15. On the left, the specimens are in their second stage of conditioning, that is, in black bags (so the radiation does not affect the roots) placed outdoors, in the vicinity of the tailings. The photo on the right shows A. atacamensis transplanted in the tailings with the respective amendments. Only 36% of A. atacamensis specimens managed to survive on the tailings. In Fig. 6.16: Progressive change of A. atacamensis during experimentation in bags. (A) A. atacamensis freshly extracted; (B) 2 weeks after transplant; and (C) 4 weeks after transplant. A photographic sequence is presented that shows the following process: (A) A specimen just extracted to be transplanted into the tailings; (B) week 2 of transplant and (C) week 4 of transplant. As can be seen in Fig. 6.16: Progressive change of A. atacamensis during experimentation in bags.  

Fig. 6.15 A. atacamensis. Left. Weathering of the tailings. Right CMZ tailings transplant site.

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(A)

(B)

(C) Fig. 6.16 Progressive change of A. atacamensis during experimentation in bags. (A) A. atacamensis freshly extracted; (B) 2 weeks after transplant; and (C) 4 weeks after transplant.

Other species that were selected to evaluate in the CMZ phytoremediation process were:

6.6.2  A. nummularia A. nummularia is a halophyte species characterized by naturally growing in environments with excess ions, mainly sodium and chlorides. It grows easily in arid and semiarid areas, due to its tolerance to saline soils. It grows fine in deep soils with 150–200 mm of rainfall

144  Chapter 6 annually but could survive a year with 50 mm of rainfall, defying low temperatures as −  10°C. Atriplex spp are unaffected by heavy textured, or high salinity soils and water, and their frost resistance is high (El Aich, 1987). Researchers have demonstrated its capacity as a Na hyperaccumulator in sodium saline soils and its potential phytoextraction capacity of this metal. Research has also been conducted on phytoremediation of soils polluted with heavy metals (Cu, Zn, and Ni), which failed to reduce this species in the time of proven contact between the plant and the soil. However, the plant showed tolerance to soils with heavy metal contents. In synthesis, halophyte species are perfect candidates for phytoextraction or phytostabilization of heavy metals contained in soils, especially if these soils are highly saline. Fig. 6.17 shows the status of the A. nummularia specimens in the indoor nursery of the CMZ tailings. It is observed that the specimens are in excellent development conditions. These plants are in their natural substrate in which they have grown and developed. These species have been cultivated in the city; therefore, in this phase, they are conditioning to the climate and height. Fig. 6.18 shows the species A. nummularia in the process of evaluation of phytoremediation in CMZ tailings, with organic and inorganic and AMF amendments, during weeks 3, 4, and 8, respectively. In the first weeks, a progressive decay of the specimens was observed. However, the plants that managed to survive (76%) achieved an adequate development from the sixth week of transplanting. Leaves fall, and change of color of the species was observed initially, but that effect was reversed over time. In Fig. 6.19 sample of A. nummularia is shown in weeks 3 and 5; in the latter, the plant dies.

Fig. 6.17 Specimens of A. nummularia in the initial conditioning process within the tailings (week 3).

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Fig. 6.18 A. nummularia in the phytoremediation evaluation process, with organic and inorganic and mycorrhizal amendments, weeks 3, 4, and 8, respectively.

Fig. 6.19 A. nummularia in the phytoremediation evaluation process, with organic and inorganic and mycorrhizal amendments, weeks 3 and 5, respectively.

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Fig. 6.20 A. nummularia in situ CMZ tailings, a drip irrigation system, is observed.

In Fig. 6.20, the plantation of A. nummularia is observed in the tailings, which is watered by a drip system. In Fig. 6.21, several specimens of A. nummularia are observed in situ on CMZ tailings. Two indicators were determined: BCF and TF, to determine the accumulation capacity of metals of A. nummularia. The concentrations of Cu, Mn, Fe, Cd, Pb, and Zn were measured. Only the Cd presented BCF values greater than 1 when amendments were used. The low concentration of this metal in the tailings provides for the fulfillment of the TF criterion greater than 1, incomparable with the contents of Cu and Fe. Therefore, A. nummularia with the amended substrate can be considered as a phytostabilizer of Cd. Additionally, Fe is the metal that has lower BCF values. Regarding TF, Mn, and Fe with T1 treatment have a TF greater than 1. Copper always presented a lower value than the unit, independent of the amendment. Pb and Zn presented TF values greater than 1. This species has the potential as an accumulator of Pb and Zn in the aerial part, without the need for amendments. The inoculation of AMF causes a decrease in the translocation of metals from the root to the aerial part.

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Fig. 6.21 A. nummularia in situ on CMZ tailings.

6.6.3  P. tamarugo P. tamarugo Phil. (P. tamarugo), naturally found in saline environments near saltwater, such as the Salton Sea of California and the Atacama Desert of Chile, is an endemic and native tree in the Pampa del Tamarugal located in the Atacama Desert, Chile. This area has a hyper-desert bioclimate, with no rainfall, minimal relative humidity, and broad temperature variation. The elevated evaporation of the soil surface creates saline deposits. They are characterized by absorbing atmospheric humidity and their high tolerance to saline environments. The null precipitation, makes this plant utterly dependent on the presence of groundwater, developing in regions where the depth of the groundwater is close to the surface. No research has been found on the use of P. tamarugo to remediate polluted soils. However, there is much research related to the phytoremediation potential of species with the same genus, as is Prosopis juliflora. Probably, P. tamarugo has not been intensely investigated because it is endemic. Fig. 6.22 shows specimens of P. tamarugo arranged in the CMZ’s indoor nursery as the initial phase of conditioning the specimens, which have been in the field for 20 days and have not shown any changes. Fig. 6.24 shows P. tamarugo blooming on conditioned tailings after 8 weeks. Fig. 6.23 shows a photograph of P. tamarugo transplanted in the CMZ tailings at week 4 of being in contact with the new substrate, corresponding to treatment: tailing + CaCO3 + compost +  15 g m−  2 AMF, where the plants have had a good evolution over time.

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Fig. 6.22 P. tamarugo in CMZ internal nursery.

Fig. 6.23 P. tamarugo transplanted in CMZ tailings with a conditioned substrate. The treatment consisted of incorporating organic and inorganic amendments, but 15 g m−  2 AMF was inoculated.

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Fig. 6.24 Full bloom of P. tamarugo in CMZ tailings conditioned at week 8.

In the research carried out on the CMZ tailings, the P. tamarugo species showed to be an accumulator of Zn and Cd in the aerial part, not requiring the incorporation of amendments; on the contrary, the addition of amendments reduces the effectiveness of metal translocation towards the top of the plant, favoring the phytostabilization process at the roots. Regarding the BCF, it was higher than the unit value, only for Cd undergoing T2 treatment, again it is important to reiterate that for tailings, it is challenging to find values on the unit for BCF, considering the high concentration of metals in the tailings. However, for the specific case of Cd, is this possible, since the overall concentration of Cd in the tailings is low, even in some cases, the available instruments could not detect it. Considering the case of BCF for Cd in untreated tailings, the value of BCF is 0.33, which is comparable with the value of BCF obtained for Cu and Zn with tailings submitted to T2 treatment; the highest BCF values correspond to Cd first, seconded by Cu and Zn. Concerning the translocation factor values, Mn, Zn, and Cd obtain values higher than the unit ones; therefore, it would be a potential accumulator of these metals under certain conditions: Mn and Cd with T1 treatment; Zn without treatment.

6.6.4  G. rigens G. rigens is a species of herbaceous plant that belongs to the Asteraceae family. It is native to South Africa and Mozambique. It has been adapted in other parts of the world and is grown as an ornamental plant. Gazania tolerates dry and hot environments, has low-risk requirements, can be used in a landscape watered with saline waters, despite

150  Chapter 6 their reduction in growth rate, they did not present any injury symptoms, the tailings under study are highly sodium saline; therefore, these species choose to evaluate. It can be grown in arid soils, as it is a plant that tolerates drought. It adapts to any type of soil, also weak, but utterly draining, can withstand long periods of drought and high and low temperatures, up to about −  10°C, in arid climates; The speed of growth and early flowering allow it to be grown as an annual in unfavorable climates, particularly those with cold and wet winters. There is little research that shows the potential of the G. rigens species to treat contaminated soils; however, within the few that exist, they have demonstrated its high tolerance to hydrocarbons. Regarding the use of this species in soils contaminated with heavy metals, tolerance to soils containing lead has been seen. Fig. 6.25 shows species G. rigens in the process of phytoremediation evaluation of CMZ tailings conditioned with organic and inorganic amendments for 4 weeks. The BCF was determined, obtaining values less than 1 for Fe, Mn, Pb, Al, and Zn, thereby demonstrating that G. rigens acts as an exclusive for these metals. On the other hand, the BCF values for Cu fluctuated between 16.29 and 49.72 for this metal, thus constituting G. rigens as a Cu accumulator. In the case of Cd, given the small concentrations, it could not be detected. For Fe, BCFs were affected between 16% and 37%, not very significant due to BCFs are small. For Mn, the largest BCF was obtained for the tailings alone, without amendment; when applying amendments, a decrease between 33% and 50% is observed. For Al, the incorporation of amendments causes a decrease between 49% and 58% of the BCF. For Pb and Zn, there is no effect of the amendments.

Fig. 6.25 G. rigens when in contact with the tailings conditioning at week 4.

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6.6.5  P. hortorum P. hortorum is an ornamental plant, which has been investigated for its potential to remedy soils contaminated with heavy metals, including Cd, Zn, Cu, Cr, Ni, and Pb. Other research reveals the potential of the P. hortorum species for phytoremediation systems on soils contaminated with Cd, Ni, and Pb. Other investigations apply amendments to improve the bioavailability conditions of Cd. According to Lam and collaborators (2018a,b), the P. hortorum species behaved as an exclusive of Fe, Mn, Pb, Al, and Zn, while presenting characteristics such as potential accumulators of Cu. The amendment with AMF had a positive effect on the adaption of P. hortorum, and this effect increased with the use of organic or inorganic amendments. The concentration values of Cd were minimal, illegible by the measuring equipment. In the case of Cu, the BCF values were 8.35–10.50. The highest value was obtained for the tailings without amendments, determining that P. hortorum is Cu hyperaccumulator. Fig. 6.26 shows specimens of G. rigens and P. hortorum in nursery inside CMZ, in the process of height adaptation, since the plants were brought from the city to the site. Once the conditioning time of the specimens of both species in the nursery is over, they are taken outdoors (see Fig. 6.27) to acclimatize with the local environmental conditions (temperature changes, winds, among others). A specimen of P. hortorum in situ (CMZ tailings) is shown in Fig. 6.28.

Fig. 6.26 Specimens of G. rigens and P. hortorum in nursery inside CMZ.

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Fig. 6.27 Specimens of G. rigens and P. hortorum outside CMZ.

Fig. 6.28 P. hortorum in situ in CMZ tailings.

6.6.6  S. molle S. molle, a native tree that is found between the regions of Tarapacá to Coquimbo (Chile), also, in other countries of South America. It is a species adapted to dry and arid environments, although it acclimatizes well to the Mediterranean climate of the Central Zone of Chile (García Berguecio and Ormazabal Pablioti, 2008). It grows in quite arid and saline soils, with

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Fig. 6.29 S. molle in CMZ indoor nursery.

intense insolation and very resistant to drought, but little tolerant to excess irrigation and saline environments. Fig. 6.29 shows a sample of S. molle specimens in CMZ indoor nursery for the initial conditioning of specimens. BCF values were lower than the unit value for Cu, Mn, Fe, Pb, and Zn, indicating that S. molle is exclusory of these metals. For the Cd, as mentioned for the rest of the cases, the concentration is low, and even in most sampling points it could not be detected by the measuring equipment; however, for tailings treated with T1, the BCF value rose from 0.42 (untreated tailings) to 3.36 (tailings exposed to T1), showing this species as a Cd extractor. Regarding the values of TF, for Cu, Mn, Pb, and Zn, were obtained on the unit for specimens planted on untreated tailings, demonstrating their ability to accumulate these metals. In the case of Fe, for all cases, TF values were lower than 1. In the case of Cd, the concentration could not be determined. Fig. 6.30 shows specimens of S. molle in the phytoremediation evaluation process, with organic, inorganic, and mycorrhizal amendments, in week 2 (left) and week 3 (right), respectively. Finally, there are introduced species from the organic amendment, which were monitored growing under tailings conditions; in 4 months, it reached a height of 47 cm, a radius of

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Fig. 6.30 S. molle in the phytoremediation evaluation process, with organic, inorganic, and mycorrhizal amendments, in week 2 (left) and 3 (right), respectively.

35 cm, and about 32 branches. The species corresponds to a Melilotus sp. The outbreak of this specimen arose before the arrival of spring, so the behavior that it may have in the tailings during winter is unknown. Figs. 6.31 and 6.32 show the development of the species between September and February. No metal analysis was performed. Mine tailings phytoremediation focus on the selection of tolerant plants, soil amelioration, and soil microorganisms’ role (Wang et al., 2017). Selecting the appropriate plant species should consider their high level of tolerance to metal, extreme soil conditions (high salinity,

Fig. 6.31 Appearance of Melilotus sp. in CMZ tailings (September).

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Fig. 6.32 Appearance of flowers and seeds of Melilotus sp.

alkalinity or acidity), present dense rooting systems, high biomass production, and fast growth rates (Wang et al., 2017). In arid and semiarid zones, it must adjust to drought. Metal-tolerant native plants are often chosen due to their tolerance to regional environmental conditions; therefore, they could easily grow and proliferate (Santibañez et al., 2012; Wang et al., 2017). Plants suitable for phytoremediation can be classified base on their work as metal hyperaccumulators and biomass producers. Hyperaccumulators present higher levels of metal ion adsorption, not typically produce high amounts of biomass, and develop a slow growth rate. Biomass producers show high biomass generation and growth rates, with low metal uptake capacity (Wang et al., 2017). As an example, the trend of the TF of four metals by species A. nummularia, P. tamarugo, and S. molle are presented in Fig. 6.33 considering the three treatments evaluated (T0, T1, and T2). It is observed that the S. molle species had a TF high value was obtained for the Cu considering the tailings alone, without conditioning it with amendments. In the case of A. nummularia, for treatment T1 the highest value of TF was obtained for Pb. Comparing the three plants evaluated, the one with the lowest TF values on average was P. tamarugo, and the one with the highest TF values on average was S. molle. The trend of the bioaccumulation factor, BCF, is shown in Fig. 6.34. The one with the highest value was Zn using P. tamarugo and S. molle. On average, the species that presented the highest BCF value was A. nummularia. Fig. 6.35 shows the concentrations of the tailings subjected to different treatments and exposed to three plant species (A. nummularia, P. tamarugo, and S. molle). In Fig. 6.35 the last bar represents the initial concentrations of the untreated tailings without being subjected to the phytoremediation process. This mine tailings initial conditions show a high concentration of Fe, and in a lower concentration, but also high, copper is found,

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Fig. 6.33 Translocation factor of Cu, Fe, Pb, and Zn in selected plants for different treatments.

Fig. 6.34 Bioconcentration factor of Cu, Fe, Pb, and Zn in selected plants for different treatments.

both correspond to the tailings main metals content. Fig. 6.35 shows that the highest bars represent, for the tailings submitted to phytoremediation, correspond to copper and not to Fe as might be expected, which indicates that much of the Fe was mobilized towards the plant.

6.7  Limitations of phytoremediation of mine tailings in arid and semiarid regions The main constraints to the formation and growth of plant cover on mine tailings are the elevated concentration of potentially toxic elements, toxic to most plant species, the small levels

Mine tailings phytoremediation in arid and semiarid environments  157

Fig. 6.35 Mine tailings chemical characterization after metals treatments.

of organic matter, nutrients, and water retention (Vangronsveld et al., 2009; Sánchez-López et al., 2015b). Mine tailings have numerous limitations degrading soils physical properties that obstruct the vegetation growth, such as shallow organic matter content, high concentrations of metals and metalloids, sharp acidity, eolian dispersion, water erosion, soil compaction, low porosity, and high salinity (Mendez and Maier, 2008; Martínez-Pagán et al., 2011; MartínezMartínez et al., 2013; Moreno-Barriga et al., 2017a,b). Therefore, some species are tailored to the extreme edaphic conditions, and these species might be suitable for phytoremediation (Mendez and Maier, 2008; Barrutia et al., 2011; Sánchez-López et al., 2015b). The irrigation number and amendment had a significant influence on electrical conductivity (Lam et al., 2016). Mine tailings’ adverse conditions include a high concentration of metals and salts, low organic matter content, and an unbalance rate of nutrients, limiting the vegetation development (Acosta et al., 2018). Vegetation germination and growth directly on mine tailings and polluted soil can be challenging, particularly in regions with a Mediterranean climate; when the plants’ growth is slow, it limits the environmental rehabilitation success (Santos et al., 2019). Greenhouses allow plant establishment of compost amendment and seeding for sustained plant growth (Wang et al., 2017). The study made by (Lam et al., 2018a) shows that inorganic and organic amendments do not significantly affect G. rigens and P. hortorum adaptation, indicating that both species can adapt without amendments. However, the mycorrhizal influences the adaption of P. hortorum, and it is increased by the use of inorganic or organic amendments (Lam et al., 2018a). In areas of arid conditions, the inorganic amendment was the least successful treatment in reducing salts. Consequently, this amendment does not help diminish salinity in tailings (Lam et al., 2016).

158  Chapter 6 In summary, phytoremediation is a lengthy process taking several years or even longer to clean up the area, most of the hyperaccumulators grow slowly, and it is only applicable to surface soils (Laghlimi et al., 2015; Mang and Ntushelo, 2019). It is seasonally dependent, in a high concentration of pollutants, can be toxic for plants, restrictive for areas with low contaminant concentration, and it is not capable of reducing all the pollution, demanding a technical strategy to choose the proper species that grow in certain places in the presence of metals. Additionally, mismanage can risk food chain contamination (Laghlimi et al., 2015). Multielement and organic pollutant presence make the process more challenging. Climatic conditions can be a limiting factor, especially when metals are dragged by rain back into the soil by the plants’ decomposition biomass. The application of nonnative species disturbs the local biodiversity (Laghlimi et al., 2015). The ability of plants to collect metals from soils can be estimated using a BCF, the proportion of metal concentration in the shoots, or roots concerning that of the soil (Sigua et al., 2019). Bioconcentration values in the corn amendment of Cd and Zn were significantly higher than one on mine contaminated soil. This indicates that Cd and Zn were highly bioaccumulated and phytostabilized in mined fields thanks to biochar and phytostabilization with corn amendment (Sigua et al., 2019). Plants with hyperaccumulation ability must have a translocation factor and a BCF of more than one (Cluis, 2004; Wei and Zhou, 2004; Brooks, 1994; Afonso et al., 2019). The criterion greater than 1 for BCF should not be used when conducting studies in heavy metal concentration environments that are as high as found in mine tailings, as this would be difficult for the concentration to be highly bioavailable metals in tailings could correspond to the concentration of metals in plants (Lam et al., 2018a). The species have different roles based on the specific conditions where they are growing at one site performing as a potentially toxic elements accumulator and at another as a stabilizer — therefore, due to the absence of a consistent approach for interpretation and calculation of bioaccumulation factors, only considering bioconcentration and translocation factors maybe not practical in all cases (Sánchez-López et al., 2015b).

6.8 Conclusions Physical treatment involves dumping, covering, or solidifying to enhance soil conditions and prevent contaminant migration, offering a suitable substrate for plant growth. Chemical remediation involves soil washing, leaching, and acid extraction, used to eliminate heavy metals with organic chemical reagents. Chemical treatment, compared to physical restoration, is effective to repair fast, and it is valid as an intensive treatment in minor facilities with heavy pollution, however, impoverished the physical properties of the soil may be. Bioremediation, particularly, phytoremediation diffuses polluted areas using plants by detoxifying and

Mine tailings phytoremediation in arid and semiarid environments  159 removing, reducing the exposure risk. However, chemical, biological, and physical mine tailings properties limit the plants’ growth. Biotechnologies for the rehabilitation of mine waste and soils lead to sustainable and integrated waste management, because of their chemical and physical characteristics, safe for land applications, low cost, waste valorization usually deposited without treatment, and reuse of organic matter and nutrients. The phytostabilization process decreases contaminants’ bioavailability, mobility, and solubility; however, the pollutants’ total concentration in the soil is not reduced. The current regulations in force in Chile are considered significant advances in the sustainable development of the national mining industry, which is world class. Responding if it is possible to achieve fully sustainable mining which is difficult and perhaps impossible. Nevertheless, it is feasible to move towards sustainable development, making improvements in national environmental legislation, which will allow shortly to achieve and then exceed the standards of world class. A genuine advance to sustainable development will be achieved to the extent that companies assume the responsible role of the future of the waste generated in the processes, throughout the entire life cycle of the mining project, proposing a closure plan as an intrinsic part of the mining project, which must be designed at the beginning. The closure plan must be implemented progressively from the earliest phase of the project, which must be updated as the mine’s operational life develops, ensuring the closure of operations in a sustainable manner. It is required to establish a link between the appropriate stakeholders, to develop precise tools with specific indicators and criteria, containing the regulatory framework, policies, measures, and technological improvements for the prevention and control of the negative impacts of any mining process, as well as the influx of new capitals destined to improve and optimize the use of natural resources. The mining sector must internalize the duty to leave the mining site in the same or better conditions than those found before the development of the mining project, which must be carried out progressively.

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CHAPTE R 7

Phytoreclamation of abandoned acid mine drainage site after treatment with fly ash Madhumita Roy Department of Microbiology, Bose Institute, Kankurgachi, Kolkata, India

7.1 Introduction Since the dawn of the industrial revolution, human beings are burning more and more fossil fuels, releasing more greenhouse gases (GHGs) into the environment. GHG by trapping more solar heat energy are responsible for increasing the planet’s temperature and causing climate change. Present day natural calamities like stronger hurricanes, harsher heat waves, and enhanced melting of the permafrost may be a consequence of this global warming. Despite the threat of global warming and climate change, global energy demand is continuously rising and the finite reserves of fossil fuels like oil, coal, and natural gas are getting harder to extract. Drilling and mining techniques are getting more invasive, and the environmental impacts of fossil fuel burning are rapidly rising. Along with creating new mining sites and abandoning used ones, the amount of fly ash (FA) which is the byproduct of coalburning is increasing at a rapid rate. Destruction of new land and habitat due to mining and drilling activities and leaving the abandoned ones without restoring them to the original state is aggravating the problem of land management. Drilling and mining practices have a substantial long-lasting negative effect on local water sources, biodiversity, disease, and health and natural resources due to pollution and land degradation. So mining, oil drilling, and FA generation these three activities associated with burning of fossil fuel are causing major global environmental problem affecting the health and well-being of millions of people worldwide. Of the many environmental, wildlife, and human health risks associated with the extraction and burning of fossil fuels, the most dangerous and potentially irreversible consequences are the emission of GHG. For example, in 2014, ~  78% of US global warming emissions, composed of carbon dioxide, were energy-related emissions and out of this, ~  42% came from oil and other liquids, 32% from coal, and 27% from natural gas (EIA, 2015). Among the fossil fuels, coal is the world’s largest energy source, burning of which generates a huge volume of coal FA, posing another risk of disposal (Izquierdo and Querol, 2012). Globally, many efforts have been done to recycle the 7.8 billion tons of coal ash currently Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00018-2 © 2021 Elsevier Inc. All rights reserved.

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168  Chapter 7 generated annually. Out of this, only 53.3% is currently recycled. Coal ash has been successfully used for a long time in a wide range of applications, including civil engineering constructions, brick making, concrete pavement, road base, embankment, structural fill, mine reclamation, soil stabilization, and fertilizer, production of other compounds like zeolites and geopolymers (Yao et al., 2015). Many countries use coal ash for mine reclamation because it can act as (i) soil amendment or substitute, (ii) alkaline amendment to neutralize acidproducing rock, (iii) encapsulation of acid-producing materials, (iv) barriers to acid mine drainage (AMD) formation/transport, (v) pit filling to reach approximate original contour in surface mines, (vi) subsidence control in underground mines, (vii) filling of underground mine voids to control acid drainage. Mining leads to complete or partial degradation of land, removal of topsoil, biodiversity loss, death of native vegetation, destruction of forest ecosystem, and fragmentation of wildlife habitat. The magnitude of devastation of the ecosystem is so massive that entire landscape of the area gets altered and a huge amount of toxic mine waste/overburden is generated that needs immediate treatment. Mine waste encompasses mine overburden, mine spoil, slag, waste rock, and tailings on land surfaces, while mine wasteland encompasses open-pits, loose soil piles, stripped areas, mine overburden surfaces, subsided lands, tailings dams, etc. (Wong, 2003; Venkateswarlu et al., 2016). AMD, the secondary effect of mining, is caused by the outflow of acidic water in the mining site. As sulfide-containing rocks are exposed to the weathering process from mining activities, certain minerals like sulfides of iron (pyrite and pyrrhotite) present in the rocks (stable and insoluble when hidden from atmospheric oxygen and water) react to form sulfuric acid upon exposure to air and water. This acid further dissolves hazardous heavy metals from the rocks. As the flowing water passes through other mining leftovers/wastes, it further dissolves and picks up metals and other substances that further pollute the downstream water posing serious threats to ecosystems. The AMD sites are considered as harmful as the acidic nature not only harms aquatic life and flora and fauna diversity of the area but the increased heavy metal content (acid causes leaching out of the heavy metals from ores) can pollute groundwater and nearby surface water of streams and rivers. AMD comes mainly from abandoned coal mines, as well as active mining sites; mine tailings (byproducts leftover from mining); mine waste rock dumps, and coal spoils/ overburdens. The heavy metal-loaded acid is carried away by rainwater or surface drainage to the nearby streams, rivers, or lakes, accelerating environmental risks. The only saving grace is that unlike other industries, mining is a temporary use of land and with proper scientific intervention, a functioning ecosystem can be restored, and in some cases, even a better landscape can be achieved. Several organizations are carrying out scientific phytorestoration work in mined out areas. Before 1970s, mining companies used to leave mine sites in the degraded states. Some abandoned mines were announced as “orphaned” as the owners could not be traced or in cases where the owner rejected to clean the mine site. In those cases, governments decided to close and rehabilitate orphaned and abandoned mines. Many

Phytoreclamation of abandoned acid mine drainage site  169 of these abandoned mining lands are beyond any commercial, recreational, or social use. But increased population pressure and economic development are demanding new mining lands. In India alone, the total land requirement for mine operation, waste dumps and mine infrastructures is projected to increase from the level of 1470 km2 (including a forest area of 730 km2) in 2006‑2007 to 2925 km2 (including a forest area of 730 km2 in 2025) as per “Vision Coal-2025” document. So it is now important to phytorestore such abandoned lands to get back fully functional ecosystem and manage new lands for new mining and keep the wheel of development running. Ultimately, the goal should be to encourage the generation and use of renewable energy resources and accelerate every country’s transition from dirty to clean energy. The landscapes damaged due to harvesting of fossil fuels can be converted into zone of clean green energy by plantation of bioenergy plants and production of biofuel in form of biodiesel, bioethanol, bioelectricity, heat energy, bio-oil, biogas, etc. However, before reclaiming the lands and bringing back the native vegetation, the damaged soil must be reconstructed. Toxic nature, scarce organic matter, less moisture and nutrient level, and other physiochemical properties of mine spoils make it unfavorable for both plant and microbial growth (Singh et al., 2004). Natural recovery of such disturbed habitats through slow colonization of plant and animal species would take much longer time and in the meantime leached out heavy metals and other pollutants and acidic discharge would harm the underground water reservoir and surface water bodies (Sharma and Sunderraj, 2005). In many cases, treatment of the mine spoil with alkaline coal ash increases pH, reverses the effect of AMD (Reynolds and Petrik, 2005), adds more carbon and plant essential nutrients and in doing so restores the soil fertility and helps in the establishment of primary vegetation. In the case of underground mining, coal ash is used as filler. Re-vegetation is supposed to be the best tool for the reclamation of mine spoils (Singh et al., 2002) and the foundation of forest regeneration on the degraded areas (Wang et al., 2007a). Re-vegetation through trees and grasses can check soil erosion and stabilize the dump slope (Singh, 2011). According to Filcheva et al. (2000), trees are better biomass generators, add more organic material (both above- and below-ground) in the form of litter deposition and humus formation to the soil and are associated with a large variety of soil microbes and earthworms (Singh et al., 2012). The deep roots of woody species penetrate a greater depth of raw mine stones in the soil organic system. Microbes associated with the roots produce different types of exudates that help better anchorage of the roots. The stability of the slope mainly depends on the properties of root systems such as the root distribution and tensile strength (Li et al., 2007). Plant roots enhance dump stability by regulating rainwater interception, decreases the pore pressure reduction (Hussain, 1995), and contributes to hydrogeological cycle regulation (Singh et al., 2012). This chapter discusses how a forest can be regenerated on a bare and topsoil cover less damaged mine lands with the help of fly ash, different types of soil organic amendments and finally native plant species. The success of mining site restoration depends on proper integration of scientific and civil/mechanical engineering knowledge with sound phytomanagement plan.

170  Chapter 7

7.2  Environmental impacts of mining and drilling and need for remediation Mining is of two types: surface mining and underground mining. The consequences of both types of mining are severe and need human intervention for removing the negative impacts of mining which last for a long time. When coal-rich veins get discovered near the surface or subsurface layer of a body of rock, mining operations are preferred above ground to reduce costs and improve extraction efficiency. This is called open-cast mining or open-pit mining or strip mining. Although, strip mining is economically feasible it causes malfunctioning of a large part of land and can wipe out the entire biologic flora and fauna on the surface of the mine. This loss of vegetation cannot stabilize, the rock later especially in forest areas, since there’s no vegetation to stabilize the rock layer. An area that went through strip-mining action can take decades to recover without intervention. In many mines, a special insoluble yellow-orange solid (colloquially known as yellow boy) formed by the reaction of iron with sulfate and/or sulfide is visible. This yellow boy is visible evidence of AMD that acts as a slow poison for the nearby aquifers. This polluted and acidic AMD water can kill life along water sources for miles. For example, the Questa molybdenum mine in New Mexico caused more than 8 miles of damage to the Red River. Other than AMD, other environmental implications of mining result from soil erosion, sinkholes, destruction of agricultural land, change in water flow system, loss of biodiversity, disturbance in soil nutrient cycling and contamination of soil, groundwater, and surface water by the chemicals released from mining processes at local, regional, and global scales. Adverse effect of mining remains for a long time even after terminating the mining activity as the mine trailing continues to emit multiple heavy metals for a long duration and the high concentration of the metals is dispersed widely by wind dispersal and water erosion (Doumas et al., 2018). Drilling of mine causes major habitat modification, not only at the exploitation site but perturbs a larger area with the mine-waste residuals contaminating the surroundings and affecting other nearby ecosystems. Destruction of the habitat is the main reason for biodiversity loss. Direct poisoning caused by inhalation of mine-extracted toxic material and indirect poisoning through consuming contaminated food and water, can also affect animals and humans. Change of habitat conditions such as pH and temperature fluctuations disturb communities of the surrounding neighboring sites. Endemic or local species are especially sensitive to these environmental modifications, as they cannot adapt to such changes. Heavy metal concentrations decrease as their distance increases from the source points (Jung and Thornton, 1996) and affect the biodiversity accordingly. Accumulation of the heavy metals in the sediments changes their speciation status as a result of oxidation or reduction. This also affects their toxicity for aquatic organisms. Heavy metals with less mobility (e.g., arsenate) will stay inert and less bioavailable while highly mobile molecules (e.g., arsenite) will easily move from one environmental compartment to another and ultimately may end up in some living body. Abandoned mines from where mining activity has stopped but left without remediation

Phytoreclamation of abandoned acid mine drainage site  171 acts as a source of pollution to all the surrounding ecosystems for a long time. Many such abandoned mines are spread over in all the Mediterranean countries (Doumas et al., 2018). Without restoring and replanting the ecosystem, an open mining site can take decades of time to recover. The slope of the abandoned mining walls can be steep or vertical, and the structural integrity of the access points constantly changes as erosion progresses. Without vegetation to stabilize the surface, rockslides, and landslides can take place without warning taking the lives of local villagers. Such incidents and loss of life have happened in many parts of the world. Implementation of proper phytomanagement with native plant species able to phytostabilize mine tailings is regarded as the more adapted green technology that can constrain the transfer of contaminants from mining waste to the different components of the environment. In some countries, there are strict environmental and rehabilitation rules and regulations that would force the mine owners to ensure that the mined area would be returned to its natural state (Hedin et al., 2005). Oil and gas production is another major culprit of environmental pollution and one of the world’s biggest killers according to the United Nations. Oil drilling produces methane: causative agent of global warming. Although the purpose of drilling is to capture and use it as the energy source, sometimes it is either vented (released) or flared (burned). Vented methane contributes directly to global warming while flaring converts the form of the gas from methane to carbon dioxide, which is also a greenhouse gas with less heat-trapping capacity than methane. When oil and gas are extracted from natural reservoirs, toxic water present under the geologic formations is exposed to the surface. This “produced water” generally is rich in heavy metals, hydrocarbons, radioactive materials, and other dissolved solids in quantities that make it not only unsuitable for human consumption but also difficult to dispose of (NRC, 2010). Extraction companies use open-air pits with impermeable liners to store the “produced water” to avoid seepage, but accidental leakage or overflow of the contents due to heavy rain can expose it again to the environment. Covered holding tanks can be a more secure temporary storage option than open pits (Zoback et al., 2010). Like AMD water from mining, oil, and gas wastewater impact aquatic life. Oil and grease leaked into water systems can adhere and damage health to aquatic animals and other organisms constituting the primary food chain of aquatic ecosystems like algae and plankton. Subsequent biomagnifications may pass the heavy metals to the higher food chain, adversely affecting human health. Like abandoned mines, abandoned oil drilling sites poses risk to the ecosystem for a long time. For instance, Hedin et al. (2005) observed that in northwestern Pennsylvania (USA), many abandoned natural gas wells were producing artesian flows of iron contaminated water. They assumed the source of water to be brine from the gas-producing sands. After sampling 20 artesian discharges with clear iron staining the waters were found to be AMD water and not brine. The mining sites had coal beds at higher elevations. It was assumed that AMD water formed in the coal mines was invading into lower aquifers, moving outside the lateral limits of mining, and using the abandoned gas wells as conduits to the

172  Chapter 7 surface. It was also presumed that the AMD chemistry was modified while flowing through the underlying sandstones by contact with siderite (the dominant carbonate mineral) in this stratigraphy. The drilling method of “fracking” involves the injection of a mixture of water and chemicals into rock formations to release oil and gas contaminates drinking water sources with carcinogenic chemicals that lead to birth defects, cancer, kidney, and liver damage. The huge volumes of dangerous chemicals laden wastewater can leak to ponds, lagoons, and underground aquifers. Drilling well and the associated roads, processing facilities, and pipelines occupy and disturb a large amount of land. By creating noise and habitat fragmentation it harms wildlife populations. For example, one study found 82% population reduction in the Powder River Basin sage grouse between 2001 and 2005, which was found to be directly associated with the area’s coal bed methane production (Taylor et al., 2012). In the unstable area of earth, drilling techniques can bring about unpredictable damage. For example, the Napoleonville salt dome extends 30,000 ft below the earth’s surface with large pillars of salt reaching upwards from the main dome. In 1982, Texas Brine Company sank a well to extract salt, hollowing out a huge cavern. This cavern is the main culprit of the Bayou Corne Sinkhole which continues to belch forth flammable methane gas and has wiped out entirely the local community. The sinkhole was capped in 2011. Extracting oil sometimes brings the most undesirable environmental consequence of uncontrolled oil spills. The event of an uncontrolled oil spill can happen during any stage of the several phases of oil extraction, drilling, and transport. Water bodies and aquatic life would be the direct sufferer of such an event. Deepwater Horizon Oil Spill in the Gulf of Mexico in 2010 was one of the most deadly examples of the impact of a large-scale oil spill. 4.9 million barrels of oil were leaked over 3 months, perishing thousands of marine mammals, seabirds, fish, and crustaceans that made up the Gulf’s ecosystem. Billions of dollars were given out to remediate miles of ocean and coastline. Offshore oil and gas drilling poses almost the same risks as onshore drilling; however, these risks are amplified due to the remote location of offshore drilling sites and the complicated engineering required. In 2010, at the Deepwater Horizon offshore oil rig in the Gulf of Mexico, an explosion took place that killed 11 workers and caused the release of ~  4.9 million barrels of oil over 87 days (OSC, 2011). Although an accident of this huge scale was unique, many small and scattered environmental and safety incidents are common in the offshore oil and gas industries. Between 2008 and 2012, offshore drilling rigs bore the brunt of 34 fatalities, 1436 injuries, and 60 oil spills of more than 50 barrels each (BSEE, 2015).

7.3  Coal fly ash: Properties and use for mine reclamation Coal is the highest carbon-containing fossil fuel. Along with carbon, it contains a large amount of toxic heavy metals and other chemicals. Cleaning and refinement of the sulfur-rich coal involves crushing and washing to remove waste products before it is transported to the thermal power plant (TPP). It leaves behind coal slurry, a semi-solid/semi-fluid waste that contains arsenic, cadmium, chromium, lead, mercury, and other heavy metals. As much as

Phytoreclamation of abandoned acid mine drainage site  173 50% of pre-processed coal materials can end up as highly toxic waste (NRC, 2010). Before combustion the coal slurry and after combustion the coal ash both are stored in large reservoir impoundments. The US alone has 1000 coal slurry impoundments and coal ash landfill sites and many of them possess hundreds of millions of gallons of coal ash either in wet (slurry) or dry form (Eilperin and Mufson, 2013). Unlined reservoirs (42% of US coal combustion waste ponds and landfills) pose a greater risk than lined reservoirs for leaching of harmful chemicals into surface and groundwater supplies and consumption of such water may cause heavy metal toxicity in the human body. Over the last several decades, several dozen spills have occurred in such reservoirs in Appalachia, including the Duke Energy Dan River Spill (2014), Tennessee Valley Authority spill (2008), Martin County Coal Company spill (2000), etc. (Epstein et al., 2011). When the coal is burned, the harmful materials contained in it are released as coal ash which is composed of 80% fly ash and rest bottom ash (19%–20%) and boiler slag (0%–1%). Fly ash (80%), bottom ash (20%), and the boiler slag (  20% lime, it is very good for acidic soils, and coal refuse or coal waste materials to stabilize the acid and absorb heavy metals on its surface (Jiangjiang et al., 2010). FGD material is highly suitable in areas with high sodium content or in sodic soils (Rhoton et al., 2011). In the earliest study on the use of FA for reclamation, Capp and Adams (1971) first found that the addition of FA to acidic mine soils permitted the growth of grasses and legumes, changed the soil pH tolerable for plant growth, added new plant essential nutrients to the soil, escalated the texture of the soil, and increased the water holding capacity of the resulting mixture. Stehouwer et al. (1994) also reported that the application of FGD materials at heavy rates to acid mine soils improved soil pH and growth of forages. They found that soil pH increased when the material was added at 0.5, 1.0, and 2.0 times the lime requirement and yield of

Phytoreclamation of abandoned acid mine drainage site  183 alfalfa and corn were improved. They found no detrimental effect of FA on soil quality during the period of the study. Hu et al. (2004) observed FA amendment at 1% and 5% application rates improved soil and plant growth conditions on mine soils in China. He also noticed that the addition of poultry litter with FA further increased plant growth and yield. The addition of poultry litter significantly decreased concentrations of Zn and Cu in soybeans while the addition of 5% FA alone caused only a slight decrease in Zn and Cu. Soil containing abandoned coal mine waste was amended with FA at high rates in South Korea (Yang et al., 2011). Spoil pH increased from 3.1 to 6.8 with FA addition at 40% ratio. It neutralized AMD and reduced heavy metal solubility. Grass growth on amended coal waste increased from 0 to 10 cm in length to 32–61 cm. American Electric Power and Ohio State University used FGD material to amend coal refuse in fields and laboratory studies at the Rehobeth site. The FGD material showed a neutralizing potential of 15% CaCO3 equivalency and permeability of 1 × 10−  6 cm/s. The FGD material contributed a larger yield of vegetation than refuse amended with agricultural lime at equivalent amounts. Water quality from the field experiments was found to be safe, while untreated (control) run-off had high acidity and metal contents. Moreover, plots where FGD materials were used, displayed reduced infiltration rates, high stability, and erosion resistance (Mafi, 1995).

7.5  Phytoremediation of fly ash treated mine site and construction of a phytocover Mining sites have features that prevent their natural colonization by vegetation. Various authors, who have studied mine spoil physiochemical features, reported that mine spoil characteristics differ widely due to the differences in mineralogical substrates and composition of mine residue which can come from different ore minerals and veins as well as from the exploitation procedures, plant cover, and climatic conditions (Smith and Sobek, 1978; Gomez-Ros et al., 2013). The pHs of the mining wastes have been recorded as 2.5 (Conesa et al., 2006), 3.14–3.30 (Bes et al., 2014), 4.2–4.7 (Santos et al., 2016), 6.6–7.3 (Conesa et al., 2006; Randjelović et al., 2016; Parraga-Aguado et al., 2014) to 8.2–8.7 (Gomez-Ros et al., 2013; Fernandez et al., 2017). Furthermore, the range of EC is also wide (Gajić et al., 2018; Smith and Sobek, 1978). The values of organic carbon in different mine sites have been recorded as 0.5% (Conesa et al., 2006), 0.17–0.48% (Bes et al., 2014), 1.55% (Randjelović et al., 2016), 3.14–6.65% (Parraga-Aguado et al., 2014), 15.1–33.3 (Santos et al., 2016) and total nitrogen as 0.04% (Bes et al., 2014), 0.29–0.62% (Parraga-Aguado et al., 2014), 0.5–1.2% (Santos et al., 2016), etc. The mine tailings showed multi-metal pollution with high total concentrations of As, Cd, Co, Cu, Fe, Hg, Mg, Mn, Ni, Pb, Sb, Zn that exceed safety values and they largely depend on geochemical partitioning (Gomez-Ros

184  Chapter 7 et al., 2013; Parraga-Aguado et al., 2014; Bes et al., 2014; Randjelović et al., 2016; Santos et al., 2016). So without human intervention, it would take decades for the lands to return to their pre-mining states. But phytoremediation is a technique that can accelerate the process of recovery. So in the following section, a brief discussion has been made on different phytoremediation techniques, of which phytoextraction and assisted phytoextraction are more relevant in the mining site reclamation context.

7.5.1  Different types of phytoremediation Phytoremediation is an environmentally friendly, inexpensive newly evolving field of science and technology that uses evapotranspiration ability of plants (grasses/herbs/woody species) to clean up polluted soil, groundwater, and wastewater and through this procedure removes, renders or contains contaminants such as heavy metals, metalloids, trace elements, organic compounds, and radioactive compounds from the soil (Raskin et al., 1997; Salt et al., 1998; Pilon-Smits and Duc, 2009; Cunningham and Lee, 1995). Phytoreclamation of FA disposal grounds, ash ponds (Pandey et al., 2014), mines (Singh et al., 2012), and other industrially polluted sites (Mishra et al., 2020) has been widely applied with documented successes (Mpofu et al., 2013). It is becoming popular among the public and in most cases is less expensive than traditional treatment technologies such as incineration, bioslurry composting, etc. Different plants phytoremediate through different mechanisms like phytoextraction, phytostabilization, phytotransformation, phytovolatilization, and phytodegradation (Roy et al., 2015). Phytoextraction: Plants can uptake contaminants from soil or water through roots, transfer them to other parts and accumulate (either underground or aboveground biomass or both) them through the formation of chelates and sequestration of the metal(loid)s in the vacuole of cells of root or shoot or leave (Roy et al., 2015). One subtype of phytoextraction is rhizofiltration by which hydrophytes or hydroponically grown plants use their roots suspended in water to uptake or absorb the pollutants from water and bioconcentrate or precipitate them in the root or translocate and store them in shoots or leaves (Verma et al., 2006). Plants able to phytoextract are either accumulators or hyperaccumulators based on their abilities to accumulate pollutants. A hyperaccumulator is a special metallophyte plant capable of growing in soil or water with extremely high concentrations of metals, absorb these metals through their roots, and accumulate them in their tissues in extremely high concentrations (Roy et al., 2015). Generally, hyperaccumulators have a slow growth rate and low biomass (Pilon-Smits and Duc, 2009). But in contrast to hyperaccumulators, accumulators (accumulate pollutants in less concentrations than hyperaccumulators) are more suitable for phytoextraction as they have fast growth, high biomass, extended root system, high root-shoot transfer, and good tolerance to high concentrations of metal(loid)s in the plant tissues. Although phytoextraction of the heavy metals through phytomining, is a conceivable

Phytoreclamation of abandoned acid mine drainage site  185 way of recovering the material, may cause potential leaching of the compounds into the subsoil or groundwater and also carries the risk of transfer of the metals to the food chain. Phytodegradation and phytotransformation: Phytodegradation is the complete degradation of the xenobiotic compounds by plant processes or plant-associated enzymes, bacteria, and other microflora. Some pH resistant endophytes living within plant endosphere can degrade PAH compounds taken up by the plant from soil or water. Sometimes plant enzymes degrade them partially or transform (incomplete degradation) them to a less toxic state called phytotransformation. Phytovolatilization: Some heavy metals and organic pollutants can escape the atmosphere either in intact form or after going speciation through plant foliage after taken up by the plant. Examples include volatilization of mercury (Natasha et al., 2020), TCE (Limmer and Burken, 2016) etc. Phytostabilization: Phytostabilization is the in situ immobilization or containment of the contaminants in the plant rhizosphere zone. Plants with extensive root systems can reduce soil erosion to a large extent and in this procedure immobilize the heavy metals and other compounds present in the soil. It is an intermittent way to prevent leaching of harmful chemicals or heavy metals from entering groundwater. In addition, phytostabilization revamps the characteristics of the polluted soil by increasing the organic matter content and boosting up nutrient levels and preventing wind erosion. Phytostabilization is achieved by “excluders,” category of plants (limit the uptake of pollutants) (Baker, 1981). The main mechanism of phystostabilization is based on root cell denial to allow the entry of the pollutants within them and/or their further transport. Mycorrhizal fungi and the root exudates in the rhizosphere help the pollutants to stay at the outer surface of the cell wall (Pilon-Smits and Duc, 2009). In this way, most pollutants are immobilized at the root zone of the plants and not transported to the above ground parts. Presently along with using plants for phytostabilization, other minerals or organic substances are added to the soil that further assist the plant for containment of the pollutants. For example, addition of biocharas a soil amendment during multi-metal remediation of a mine site by Salix species showed arsenic and lead accumulation in roots and low translocation toward edible parts, i.e., stems and leaves proving the phytostabilization potential. It also improved soil physicochemical properties and reduced Pb soil pore water concentrations (Lebrun et al., 2018).

7.5.2  Ecorestoration and development of phytocap Ecological restoration is a term that defines a broad set of activities and incorporates enhancing, repairing or reconstructing degraded ecosystems and optimizes biodiversity returns. Benefits of ecorestoration involve erosion control, re-vegetation, re-forestation, removal of nonnative plants and weeds, and reintroduction of native species, and habitat and

186  Chapter 7 soil condition improvement for the targeted species. Ecological restoration with biodiversity benefits in mind needs to be innovative as different areas represent unique circumstances. The objective should be restoring the pre-mining ecosystem, and the following factors should be considered: cost-benefit analysis, speed of attainment, achievability, and long-term stability with ongoing management at a reasonable cost. The mining companies should understand that simple reclamation of mined-out land by planting some fast-grown trees will not serve the purpose of recovery of degraded land. Instead, the target should be rebuilding the ecosystem through ecological restoration (Rathfon et al., 2005). It has been experimentally proved that biodiversity could be restored by ecological restoration only (Ahirwal et al., 2016). For successful ecorestoration, selection of plants, soil fertility and nutrients presence, soil moisture availability, soil texture, pH, and salinity (Purdy et al., 2005; Zipper et al., 2011; Davis et al., 2012; Huang et al., 2013) all are important. The following section discusses the important factors needed for re-vegetation. Soil moisture and quality: The importance of soil moisture on re-vegetation can be seen in the re-vegetation sites of the northern hemisphere. For example, the northern aspect of hillsides offered greater soil moisture, more rapid and dense establishment of vegetation than the opposite side which was relatively dry. Soil chemical property determines revegetation success. Soil liming by way of FA addition and fertilization make mine soils more favorable for plant cover establishment under limiting conditions (Grant et al., 2007). Mine soils with high levels of heavy metals can be treated with chemical chelators to reduce their bioavailability or metal tolerant plant species can be chosen that would immobilize the contaminants. However, plants that phytoextract metals and store them in foliage should be avoided (Wong, 2003). Reconstruction of top soil: Cases where mining activities has caused total loss or damage to top soil, it should be reconstructed. There are a variety of methods for top soil construction (see detail methods of topsoil construction in Maiti and Ahirwal, 2019) including amendment with FA. Mine overburden:- Various kinds of mine overburdens affect physical and chemical features of the developing soil which in turn influence the re-vegetation success. This is particularly well documented by the reclamation of coal mining sites in the eastern USA. Early reclamation efforts (1930s–1970s) experienced planting of trees into loose, uncompacted weathered overburden (Zeleznik and Skousen, 1996; Ashby, 1998). These abandoned mining sites displayed luxurious tree growth and rapid recruitment of adjacent native trees resulting in diverse fauna after 10–20 years (Skousen et al., 2006). Influence of mine soil properties on tree growth was shown by many authors (Ashby, 1998; Zeleznik and Skousen, 1996). Although FA supplements soil with many plant growth-promoting macronutrients and micronutrients, it lacks organic carbon, phosphorous, and nitrogen. So after treatment of the AMD/mine spoil with FA, prior to plantation development, the addition of various

Phytoreclamation of abandoned acid mine drainage site  187 supplementations such as biofertilizer, organic manure, vermicompost, bio-char, etc. may be necessary (Juwarkarr and Jambhulkar, 2008) for construction of a soil cover. After construction of a soil cover, the next strategy should be the development of a plant cover through a proper phytomanagement program (Sencindiver and Ammons, 2000). The first step of mine site reclamation is the establishment of the initial colonization of grass and legume species (Skousen and Venable, 2008). For the initial establishment of grass cover, strategies such as supplementation of organic carbon and spreading of grass legume fodder seeds (for future nitrogen fixation), forage legumes, tuft, or hardy grasses have proven affective. The grass legume cover helps in the formation of a vegetation mat in a short time (Pandey et al., 2014; Prasad, 2014). During this time nitrogen fertilizer may be added as like soil organic carbon, nitrogen is another major limiting factor on mine spoils, and initial addition of nitrogen-rich fertilizer is required for establishing vegetation on mine sites. Introduction of legumes and other nitrogen-fixing species can also add soil nitrogen. Plant species that are sown or planted initially colonize mine waste deposits and bind substrate with a fibrous root system, and slowly they spread by seeds and rhizomes forming dense vegetation cover. In the initial phase of colonization, annual, and biennial plants (mainly grass species) are dominant. They are characterized by re-selection and with them, the process of vegetation regeneration starts. They enhance the fertility of the soil, prevent erosion and emission of air pollutants, and also immobilize the heavy metals. This paves way for long-term management and gradual restoration of the degraded site. The fibrous nature of the grass roots is effective in slowing down erosion and preserving soil moisture. They increase organic compounds in soil upon which other leguminous crops grow and add nitrogen. Grasses and legumes play great roles for the formation of nutrient-rich top soil. Native species of grasses can adapt very well with the prevailing environmental conditions, grow fast, increase soil fertility, and provide a sustainable microclimate for establishment of economically important species. This gives economical return from the rehabilitation programs (Karaca et al., 2018). Recently, Pandey et al. (2014, 2015) and Żołnierz et al. (2016) have shown various naturally growing species on various FA deposits. Most significant of them were naturally growing species are Saccharummunja (Pandey et al., 2012), nodulated species of chickpea (Pandey et al., 2013), nonnodulated species Cassia siamealamk, and Pteris vittata, an Ashyper accumulating fern (Srivastava et al., 2005). S. munja and Ricinus communis L., are the two most important naturally growing grass species on FA land fill sites and other degraded lands like mine sites of tropical and subtropical climates (Pandey et al., 2013). Stiles et al. (2011) conducted phytoremediation study on a land damaged by boron (B) mining in southern California. A native grass, Puccinelliadistans, which exhibited extreme tolerance to B showed its success as vegetative cover for the phytorestoration of the B mine (Stiles et al., 2011). According to Grime (1979), biennials can be competitive ruderals (C-R), and stress-tolerant ruderals (S-R). Perennial herbaceous plants grow from the bulbs, rhizomes, seeds, stolons, and tubers. The rhizomes are used for storing reserve foods during adverse periods, and act

188  Chapter 7 as a link between below ground and the above-ground shoots. Perennials can also be stresstolerant ruderals (S-R), stress-tolerant competitors (C-S), and competitive ruderals (C-R) and “C-S-R” types (Grime, 1979). Ferns like P. vittata L., Ampelopterisprolifera (Retz.) Copel., Diplaziumesculentum (Retz.) Sw. and Thelypterisdentata (Forsk.), etc. are suitable for growth on high concentration of heavy metal polluted soils without showing toxicity symptoms. Formation of a productive forest ecosystem needs gradual succession from primary annual, biennials, and perennial plant communities to secondary woody tree species that serves as the habitats for maximum biotic communities, establishes the food-web trophic levels, enhances the soil quality through leaf litter and root exudates, reduction of soil acidity and improvement of soil biological activity, increases water infiltration, prevents leaching of nutrients and other metals and allows biogeochemical cycles (Skousen et al., 2009). Shrubs and trees that can establish themselves on mine waste deposits are Acacia, Acer, Azadirachta, Albizia, Amorpha, Acacia, Acer, Cassia, Eucaliptus, Fraxinus, Grevillea, Leucaena, Meliaazedarach, Morus, Platanus, Phyllanthusemblica, Pongamiapinnata, Populus, Rubus, Rosa, Salix, Tamarix, Tectonagrandis (Cheung et al., 2000; Maiti, 2013; Gajić et al., 2016). These plants are characterized by K-selection because they have a longer life cycle and slow growth. Trees and shrubs can be competitors (C), stress-tolerant competitors (C-S), and stress tolerators (S) (Grime, 1979).

7.5.3  Forest reclamation on abandoned mines Earlier efforts to reclaim forested lands after mining disturbance often targeted re-vegetation with poor attention to landform re-creation and the use of native species or re-establishment of tree cover (Grant and Koch, 2007; Zeleznik and Skousen, 1996). However, this has changed recently. For example, the United States in 1977 enacted the Surface Mining Control and Reclamation Act (SMCRA) that caused a major change in policy of reclamation (Zipper, 2000). Initially, the focus was on reducing erosion which led authorities to encourage grading and smoothing of the reclaimed land surfaces and rapid establishment of grasses and legumes, often agricultural fodder (Chaney et al., 1995). If these lands were not used for grazing, they could naturally return to the woody vegetation, particularly on sites close to the forest (Franklin et al., 2012). But, sites with compacted soils and grass/legume dense cover inhibits establishment of forest cover for decades (Zipper et al., 2011). The Forestry Reclamation Approach (FRA) was formed to address this question in the coalfields of the Eastern USA coalfield, comprised of primarily temperate deciduous forests (Burger et al., 2005). Almost all closed-canopy forest ecosystems are composed of a complex above and below ground vertical stratification. So, for forest reclamation, reconstruction of the vertical stratification should be a fundamental objective (Skousen et al., 2006; Grant and Koch, 2007). Re-establishment of the natural closed canopy forest ecosystem consisting of native tree species help to build up a diverse native understory plant community (Koch, 2007). On

Phytoreclamation of abandoned acid mine drainage site  189 most forest reclamation sites, dependency on natural seed pollination for tree regeneration is generally avoided as tree establishment process becomes irregular and show less desirable, wind-dispersed species that tend to dominate the site and compete with other trees. Good progress was achieved with the re-establishment of native Jarrah forest in Australia through the sowing of diverse native tree seed mixes and use of surface soil materials (Grant and Koch, 2007). The target for forest site recreation is to rapidly establish a continuous tree canopy to suppress the growth of shade sensitive, “weedy” herbs and shrubs that could block growth and development of native forest understory vegetation (Macdonald et al., 2015). Tree species like Scots pine (Pinus sylvestris L.), European oak (Quercus robus L.), alders (Alnus ssp.), and European larch (Larix decidua Mill.) are popular in Central and Eastern Europe for the reclamation in mining sites (Pietrzykowski, 2019). Depending on the adaptive differences of the tree species to stressful habitats, they are classified as pioneering species and climax or late successional tree species (Frouz et al., 2015). This classification follows the classical succession theory of Clements, in which the first stage of succession involves colonization by pioneering species (Odum and Barrett, 2005) and this paves the way for establishment of more demanding late successional species. Pioneering tree species are better adapted to tolerate stressful conditions like temperature fluctuations, a lack of organic matter and water deficits. These species are characterized by small seeds that can be dispersed by wind for pollination, while climax species tend to have a capacity for vegetative propagation, and their large seeds are dispersed from the parent tree in many different manners by the help of pollinator bees, bats etc. (Johnson et al., 1997; Wagner et al., 2010). According to experts, mixed tree species should be planted instead of single-species rows or blocks (except pines) (Rathfon et al., 2005). The presence of multiple species protects against a sudden insect attack or disease outbreak. Mixing species diversity also shoots up the likelihood that some trees will be able to thrive on all areas of the mine site and under all environmental fluctuations. Re-forestation strategies of mines should be based upon succession theory aiming to mimic primary succession. Once conditions for ecological succession become suitable it takes place independently of methods of reclamation. Microorganisms play an important role in the phytoreclamation process as they are essential for nutrient cycling, especially N, P, and C (Mummey et al., 2002) and healthy growth of plants. Microbes can be used as indicators for detecting changes in the physicochemical and biological functioning of the ecosystem during the ecological restoration process of mine tailings (Mendez and Maier, 2008; Wang et al., 2012). For example, deficiency of N in mine tailings necessitates rapid growth of nitrogen fixing bacteria (Huang et al., 2011). Moreover, heterotrophic microorganisms are needed for the establishment of ecological vegetation, and the complex plant-microbe interactions play an important role in sustaining physical structures in soil, nutrient cycling, and healthy plant growth (Mendez et al., 2007; Wang et al., 2007; Rosario et al., 2007). Yenn et al. (2014) showed how PAH degrading microbes are useful in degrading and subsequent remediation of hydrocarbon contamination

190  Chapter 7 in oil drilling sites. Oil drilling sites of Assam were contaminated with 15.1‑32.8% crude oils, and the soils had a pH of 8.0‑8.7 with low moisture contents, low soil nutrients and low levels of soil enzymes (phosphatase, urease, and dehydrogenase) and high levels of heavy metals. Bio-augmentation was performed by using Pseudomonas aeruginosa strains N3 and N4 followed by the introduction of plant species Azadirachtaindica, Gmelinaarborea, Tectonagrandis, and Micheliachampaca. A study by Li et al. (2016) highlighted the structure and diversity of bacterial communities in mine tailings with plant species by metagenomic analysis of the microbial communities associated with the mine tailings. A shift of microbial diversity and structure was noticed in the top 20 cm of the soil, which also showed a change in chemical properties such as pH, total N and total organic carbon. The study confirmed that re-vegetation increased the N content due to increase in number of nitrogen-fixing bacteria and it promoted further development of the microbial communities in tailings. In the plant microbe interactions, plants stimulate microbial communities by giving food through root exudates and the microbes, in turn, protect the plants against pathogen attacks, provide plant growth hormones, convert many plant unavailable nutrients plant bioavailable (e.g., nitrogen fixation, solubilization of phosphorous) and increase oxygen availability around roots etc. Plant growth promoting rhizobacteria (PGPR) forms a consortium of bacteria that colonize the rhizosphere and degrade pollutants more efficiently than a single species/ strain (Rau et al., 2009; Roychowdhury et al., 2018). Rhizobacteria, such as Achromobacter, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Delftia, Enterobacter, Pseudomonas, Serratia, and Streptomyces had been found to have growth promoting effect on plant species in metalliferous environments as they were able to decrease the metal toxicity by bioaccumulation and biosorption (Dimkpa et al., 2009; Roy and Roy, 2018). Even some plant species need association with some microbial symbionts for their successful germination and growth. For example, the bauxite mining site of Jarrah forests observed 75% of native plant species in a stable relationship with mycorrhiza (Jasper, 2007). The amendments added during top soil formation introduce both soil microorganisms and plant propagules (Hall et al., 2010). Plant litter layer helped in the establishment of diverse and abundant mycorrhizal communities (Jasper, 2007), which subsequently associated themselves with the roots of the litter forming plants and enhanced their growth (Averill et al., 2014). It has been observed that soil bacteria typically follow the r-strategists category of organisms adapted to take advantage of changes of resource and disturbances while fungi are slow grower and tend to be conservative K-strategists (Frouz et al., 2013b). Thus, undisturbed forest soil tends to be dominated by fungi, whereas disturbed forest soil is dominated by bacteria (Jasper, 2007). Niche below plant canopies experience the highest number of fungal biomarkers and are positively correlated with the soil organic matters (Jasper, 2007). A reclaimed site can thus be used for the site of bioenergy crop cultivation (Ussiri et al., 2019) or silviculture (Casselman et al., 2006). Recently, interest is growing in converting marginal lands to bioenergy crop production land for meeting ever increasing demand

Phytoreclamation of abandoned acid mine drainage site  191 of environment friendly biofuel from biomass and at the same time not restraining with high quality croplands which could threaten food security and soil quality. Some woody tree species ideal for silviculture are Leucaenaleucocephala, Dendrocalamusstrictus, and Eucalyptus sp. that has the potential for re-vegetation on degraded sites. These tree species gives a good economic return. Other economically important timber and plywood-generating trees that have been successfully used in phytorestoration studies are Shorearobusta, Tectonagrandis, D. sissoo, Bombaxceiba, Populuseuphratica, Eucalyptus tereticornis, Eucalyptus hybrid, Eucalyptus globules, Meliaazedarach, Populus deltoids, Tamar indusindica, and Syzygiumcumini (Pandey et al., 2009; Ram et al., 2008; Davis et al., 2012). Examples of some fuel wood tree species suitable for phytorestoration job are Acacia auriculiformis, Acacia nilotica, Albizialebbeck, Cassia siamea, Casuarinaequisetifolia, Dalbergiasissoo, and Prosopisjuliflora. In addition to their economic importance, they have nitrogen-fixing properties and excellent growth characteristics in nutrient-limited conditions. Carlson and Adriano (1991), created a new ecosystem on FA dump sites with sycamore (Platanusoccidentalis) and sweetgum (Liquidambar styraciflua), which are important timber trees. Plants that showed good growth on mine reclamation sites would be found in some reviews (e.g., Gajić et al., 2018). Abreua et al. (2008) studied two native trees Erica australis and Erica and evalensis of São Domingos for their phytostabilization potential. Iberian Pyrite Belt of copper mine, São Domingos was suffering from thousands of tons of mine waste and AMD pollution that spread over several km downstream from the mine. They found the above two species growing in the low acidic mine spoil and reduced heavy metal leaching significantly.

7.5.4  Post reclamation mine condition and evaluation of restoration success Finally, the success of reclamation should be evaluated through measuring the ecological functioning (carbon sequestration, deposition of soil organic matter, nitrogen, phosphorous, nutrient cycling, soil structure, water quality, biodiversity, pollination, and biological control, etc) and monitoring the soil leachate and the groundwater quality. Reclamation success must be determined by several parameters since no single parameter provides sufficient information for ecosystem reclamation (Sheoran et al., 2010). Reclamation of abandoned mine land is a very complex process and more research should be conducted for better management of abandoned mine sites. Ash application on all site areas should involve groundwater monitoring, except those where the reason behind ash application is just a soil additive (Roy et al., 2018a,b; Ledin and Pedersen, 1996). Otherwise, groundwater monitoring is a requisite before, during and after ash placement (Gitari et al., 2006, 2008). Soil carbon is an important indicator of ecosystem recovery and ecosystem functioning in postmining soils (Turcotte et al., 2009). Soil carbon not only supports life but also contains CO2, important GHG. Results from experiments using chronosequences post-fire and post-harvesting

192  Chapter 7 indicate that post reclamation, soil carbon takes about three decades time to go back to the predisturbance conditions in boreal forests (Norris et al., 2009), while 20 and 100 years was required by secondary tropical forests to reach to the pre disturbance level of soil carbon (Martin et al., 2013). A meta-analysis on soil organic carbon in different post-mining reclaimed soils showed that most sites took less than 20 years to return back to the pre-mining level of soil organic carbon. However, it depended on vegetation types like grassland, coniferous forest, tropical and temperate forest, deciduous forest etc., effects of temperature, and location of the organic matter like mineral soil versus litter, fermenting litter and humus layers etc. (Frouz et al., 2015). Soil microbial processes are another indicator of soil functioning in the reclaimed site. Re-establishment of decomposition and nutrient cycling processes including processes of nitrogen fixation and P solubilization is an essential reflection of post-mining forest restoration (Grant et al., 2007). A fully functional ecosystem should have a rich soil biota. Colonization of the post-mining soils by soil biota will be influenced by fauna available in the surrounding landscape, the soil substrate and the vegetation, distance of the restored site from nearby undisturbed ecosystems from where the many will migrate to the new habitat, and the migration barriers (Majer et al., 2007). Usually, it has been noticed that root feeding soil fauna dominates dry grassland soils while saprophagous fauna dominates moist forest soils (Frouz et al., 2013a). Litter properties (e.g., C:N ratio) affect humus development and, in turn, affect soil fauna composition of the reclaimed site. Soil at the bottom of the trees produces a slowly-decomposing litter with a high C:N ratio. This high tannin containing wax cuticle is colonized by a diverse soil mesoand micro-fauna and a mor type of humus forms with a thick fermentation layer which in turn supports a rich variety of fungus, bacteria, and other soil dwellers (Frouz et al., 2013a). Frouz et al. (2013c) have shown that the density of mesofauna on the reclaimed sites can attain the densities of undisturbed forest within a period of 15–20 years. Forest ecosystems that receive litter with a lower C:N ratio, soil macrofauna there plays an important role. They cause litter fragmentation, mixing and bioturbation leading to the formation of a moder or even modermull type humus whichcontains higher microbial biomass, and even higher soil carbon (Frouz et al., 2013b). Complex assessments of responses of trees to stress in habitats that form on reclaimed mine sites should take into account biomass and all important growth parameters and the mineral nutrient status. The consequence of N and P deficits may affect proper nutrients in the stands and they in turn would affect stability of reclaimed post-industrial sites. Therefore, monitoring of the stand formation and of the reclaimed forest ecosystem is necessary (Pietrzykowski, 2019). Singh et al. (2012) carried out an evaluation of the reclamation efficiency of an open case coil mine in Assam after 2, 6, 10, and 12 years of re-vegetation. Mine spoil site dump nitrogen, belowground biomass, mineral nitrogen, soil nitrogen; microbial biomass and mine dump stability of the re-vegetated mine spoil were studied. Slope

Phytoreclamation of abandoned acid mine drainage site  193 stability increased from 1.2 to 1.4, 1.7, 1.9, and 2.1 after 2, 6, 10, and 12 years. Reclamation caused a satisfactory increase of all the above parameters (Singh et al., 2012).

7.6  Some successful case studies on reclamation of abandoned mines Some global case studies are given below where FA or CCP were used for successful mine restorations. Alcoa World Alumina in Australia operates two bauxitemines at Willowdale and Huntly (largest bauxite producer). The mine pits spread across one hectare to tens of hectares. Alcoa started rehabilitating its mines since 1966 and have adopted one of the state-of-the-art rehabilitation programs after improving the rehabilitation technology with time. The sites have plantations of exoticpine trees. Alcoa has been aiming to re-establishing a jarrah forest (a hardwood tree, Eucalyptus marginata, of Western Australia) on the mined areas that are as similar to the original forest as possible. The jarrah forest is renowned for its diverse flora, and is one of the densest forests with high biodiversity like tropical rainforests. High pH coal ash (pH 9.6) was used to fill a large acidic pit in Indiana. The water quality was raised to pH 7, but elevated concentrations of As and B were found in pore waters of the fill (Kolbe et al., 2011). Arsenic transport from the filled pit was highly decreased by soil and was not found in monitoring wells surrounding the site Boron however, had a low sorption to the soil and its transport lagged slightly behind the groundwater flow. Hamric (1993) used FBC ash to seal the pit floor thus preventing groundwater from contacting acid producing shale immediately below the coal on a surface mine in northern West Virginia. The ash was also placed on top of the regarded area to reduce infiltration and to lime the soil. The results of the application showed slight reductions in the acidity of AMD coming from the mine site where ash was applied. Surface mine grouting and capping for AMD control was done in Clinton County, Pennsylvania. Between 1974 and 1977, a 15-ha surface coal was mined here (Schueck et al., 1996). Pyritic pit cleanings and refuse were buried in the backfill, resulting in severe AMD. The pyritic material was located in discrete piles or pods within the backfill. The pods and initial contaminant plumes were identified using geophysical techniques. The entire area has been reclaimed now. The Monday Creek Watershed, located in the Appalachian coal belt in southeast Ohio was rated by EPA as an unrecoverable stream as large parts of Monday Creek and its tributaries were dead due to AMD from a century old coal mining. With the efforts of more than 20 partners (e.g., EPA, grassroots organizations, state offices, universities, U.S. Army Corps of Engineers, U.S. Fish and Wildlife Service, Office of Surface Mining, and the Forest Service) and an investment of approximately $10 million, the creek was partially restored and EPA

194  Chapter 7 reversed the creek’s unrecoverable rating in 2004. The creek’s water quality has improved substantially, and people are using the area for recreation. La Sal Creek (near Utah and Colorado) started mining in the 1950s for uranium and vanadium. To reach these deposits, horizontal passageways were bored through the rock and five underground mines were created producing piles of waste materials. All of the five mines are now abandoned and water quality samples confirmed the presence of arsenic and radioactive materials in nearby surface and groundwater samples. These toxic pollutants posed a risk to local residents, tourists, and aquatic life within both La Sal creek and nearby Lion Canyon Creek. US Bureau of Land Management (BLM) began a series of steps to address and correct the problems and prepared safety and health plan in December 2002, a conceptual site model in June 2003, a field sampling plan in January 2004, and an engineering evaluation/cost analysis (EE/CA) in October 2005 and started an action in 2010. The plan included construction of a sulfate-reducing bioreactor to remove metals and restore proper ground and surface water pH; demolition of unsafe structures; sealing mine openings; stabilizing slopes; removing of lower-level radiation debris; and finally planted vegetation cover on the entire area to absorb further contamination. Ongoing monitoring and maintenance work is still going on. Ten uranium mines were reclaimed in the Red Pryor Mountains of central Montana by BLM in 2006. All the 10 uranium mines were located in the Red Pryor Mountains of south central Montana. These mines created risk and recreational exposure hazards prior to the reclamation. BLM removed ore for reprocessing, re-graded waste rock or overburden piles, and closed mine entrances and fitted them with bat gates to maintain bat populations. In India, many mine restoration works are going on. For instance, North Eastern Coalfield Ltd. is trying to reclaim the mine lands and restore natural ecosystem as a result of opencast mining operations on densely forested hills of Assam. Stability of the slope was dealt with civil engineering and mechanical calculations such as terracing, revetment and retaining walls, bamboo barricading at the slopes, stone-barriers at the bottom of dumps. Vegetation restorations through plantation of various selected native species have been attempted. Re-vegetation results were quite successful with survival of diverse species at rate > 90% (Singh and Sinha, 2007). In China, a novel environmental restoration method was devised and followed for reclamation of an abandoned limestone quarry that had deep open pit and steep palisades (Wang et al., 2018). No FA or lime addition was required as it was a limestone mine. They filled the mining pits with abandoned mine materials like rock debris, construction waste, and loess. Then they constructed artificial slopes using loess and catch waters that were built in different locations to prevent rainwater mediated erosion. Next they started revegetation of the platform and the staggered slope slabs with trees, including Rhustyphina, Robiniapseudoacacia, Calocedrusmacrolepis, and PrunusCerasifera. This method successfully restored the site and post reclamation studies are still going on.

Phytoreclamation of abandoned acid mine drainage site  195 SMCRA monitored reclamation of coal surface mines in Appalachian region. Much of this land was reclaimed using methods of surface stabilization, erosion prevention, and the establishment of herbaceous vegetation. Today, these lands are almost covered with persistent herbaceous species, (for instance Fescue and Sericea lespedeza), and a mix of invasive and native woody species with little commercial or ecological value, and most are not used or managed. From an ecological point, these lands are assumed to be in a state of “arrested succession”. To transform these lands into productive forests, forest regeneration guidelines should be followed and this should include replace the current vegetation, selection of timber, and other useful forest trees, loosening up the compacted mine soils and correcting chemical or nutrient deficiencies.

7.7  Challenges and opportunities in phytorestoration of fly ash treated mines Mining is a temporary use of land. With time all the mineral deposit would exhaust and the land would return to its original form. For sustainable development, the rehabilitation program should be designed with a goal to produce fuelwood plantation, or generation of forest ecosystem. The rehabilitation objectives should be defined in close consultation with local inhabitants, as they are the people who will have to use the rehabilitated land in perpetuity after the company’s work is over. Number of abandon mined lands, and total areas and current status must be inventoried for future restoration plans (Younger et al., 2005; Johnson, 2003). The current pool of species available for phytostabilization is little and specific to a particular metal type. So further screening of potential candidates with phytostabilization potential should be undertaken and understand their breeding plans. More research is needed on testing different types of amendments that can restore the soil qualities quickly (e.g., addition of bio-char, vermicompost etc). More documentation is needed on adverse impacts of mining on regional biodiversity and how the biodiversity is restored upon mine land restoration. Pre-mining inventory of species composition should be integrated into permitting process for mining concessions. Coal FA beneficiation for the treatment of AMD also requires the below-listed criteria, studies of which have been acclaimed toward utilization of coal ash on active mining sites. Before ash placement, certain procedural sequential steps need to be taken which would suggest successful ash placement in acid mine reclamation projects. It should be kept in mind that in every mining reclamation, application of ash is not the solution and may deteriorate the existing pollution further. Fly ash gives alkaline condition, low permeability, soil additive qualities and finally a placement alternative. It is recommended that a neutralization potential and pH ranging between 7.5 and 12 are available. For proper utilization of FA having pozzolanic properties and low permeability, it is important that the permeability under lab conditions be equal to or less than 1.0 × 10–6 cm/s. Coal ash acts as a soil ameliorant and

196  Chapter 7 makes the soil qualities better when the soil ash mixture possess a pH of 6.5–8.0 which can act as a perfect growth medium. Sometimes a mixture of bottom ash and FA is considered for use on-site; in such cases both the ash quality tests should be provided before utilization. An informative and complete soil analysis report containing data on pH, PCB, different heavy metals and nonmetals and trace elements (micro and macro) including As, Cd, Cr, Hg, Pb, Zn, Fe, Co, Ni etc. should be present when the proposed utilization of ash in the form of a soil additive is given. This opens up several potential possibilities known for efficient plant uptake process (Luptakova et al., 2010). Forestry Reclamation Approach recommends: (i) Landform reconstruction by following models of natural ecosystems and making of topographic heterogeneity at different scales; (ii) Use and placement of mine overburden, organic amendments and capping materials to encourage soil development processes and create a suitable rooting medium for native trees; (iii) Alignment of landform, overburden, topography, soil and native plants to create a target ecosystem types with great variety of diversity; (iv) Combining and optimization of seed stock types and planting techniques with early plantation of a diverse tree species; (v) Encouraging natural regeneration for re-vegetation as much as possible; (vi) Preparation of forest floor material by combining seeds of native species for speedy establishment of native forest understory vegetation; (vii) Selective and sustainable phytomanagement to encourage economic return from forest site along with moving in the desired successional trajectory. Appropriate environmental management has been enacted in many countries for use of CCP as a carbonate containing mineral for mine filling. The countries are proactively using coal ash for beneficial uses under locally suitable conditions. But there is no uniform environmental assessment standard as each country uses their own standardizations with distinctive approaches reflecting their regional characteristics and environments. In Europe, for the use of CCPs for mining and other beneficial uses, a new Waste Framework Directive took place in December 2010 called Registration, Evaluation, Authorization, and Restriction of Chemicals (REACH). This directive made each member state define CCPs as nonhazardous byproducts that can serve beneficial purposes. The producers of CCPs were ordered to register their products for bringing the products safely on the market (Feuerborn, 2011). The new law’s legal framework was established to improve waste management, promoting the prevention, reuse, and recycling of waste while exempting certain wastes from waste laws. It redefined CCP as wealth instead of being a waste if appropriately handled and put to beneficial uses. In the United States, laws and regulations on coal ash are different from state to state. For instance, in Pennsylvania, where coal ash is actively used for mine reclamation projects, legalization on the use of coal ash was done in July 1992 following the revision of the Solid Waste Management Act (1986), after which the “Guidelines for Beneficial Use of Coal Ash at Coal Mines” were developed in lines with the previous regulations. In 1997 and 1998, further

Phytoreclamation of abandoned acid mine drainage site  197 revisions were made for guidance on certification standards and methodologies on the use of FA in mining sites. In India, The Ministry of Environment, Forest and Climate Change (MoEF&CC) issued the Fly Ash notification on 14th September 1999, which was further amended in 2003, 2009, and 2016. The Fly Ash notification (1999) authorized application of FA for the purpose of manufacturing certain products like cement, concrete, bricks, and construction of embankments, roads, bridges, dams etc. within a radius of 300 km from TPPs as addition of FA in those products would give added benefits to them and at the same time reduce the disposal and storage related issue of FA. The rules also mandate the use of FA in mines backfilling or stowing of mines within a distance of 50 km. However, according to the directive few areas cannot be reclaimed using FA including (i) Flood plain area/Ecologically Sensitive Areas (ii) Agriculture land/area (iii) Cattle grazing grassland. Forest land/area reclamation needs permission and clearance from MoEF&CC as per Forest Conservation Act, 1980. The successful restoration of forest ecosystems on severely disturbed mining lands is highly encouraged. Forestry Reclamation Approach (FRA) of ARRI, addressed the following challenges for forest reclamation of mine sites: (i) proper species selection for a specific mine site is determined by its location on the landscape as landscape position influences availability of soil moisture and sunlight, (ii) landowner objectives, permission, and bond release requirements, and the mine’s location relative to species’ native ranges should also be considered when selecting trees (iii) convenient soil properties and noncompetitive ground cover are necessary on mine sites intended for re-forestation (iv) tree prescription (list of species to be planted, with planting rates, for any portion of a mine or the entire area) should be developed for the major site types of the mine that needs to be re-vegetated. Most large mines usually have several site types (e.g., dry slopes: slopes facing south and west are areas with dry conditions; moist slopes: slopes facing north and east has areas with moist growing conditions and well drained soils; flat sites: flat and rolling areas with moist growing conditions and has enough landscape relief feature either to allow water to drain out or if not well drained stays wet; wet sites: areas within and adjacent to channels and surface depressions including reconstructed streams and wetlands and areas with wet soils caused by landscape location or poor internal drainage) each of which should be targeted for planting with its own tree prescription (v) a compatible mix of early-, mid-, and late-succession tree species should be selected that will shorten the period of phytocover development time starting from bare ground to a diverse, valuable, mature forest. (vi) enough number of seedlings should be planted keeping in mind that survival rates on mine sites often average about 70% (for e.g., if 450 surviving stems or less is needed then 700 trees per acre should be planted which is equivalent to an 8 ft × 8 ft spacing). Tree stocking standards should be identified for a particular mine which depends on the survival parameters at the mine land (Adams, 2017).

198  Chapter 7 Favas et al. (2018) analyzed current problems and opportunities associated with reclamation of abandoned mine sites. In spite of all these rules and regulations sustainable mining and the re-vegetation and rehabilitation of abandoned mines are still challenging. Species selection, control and management of invasive alien species and monitoring procedures need an ongoing multidisciplinary approach. Modern functional and phylogenetic researches in community ecology have the potential to augment entire rehabilitation steps and to overcome the challenges addressed, but methodologies must be developed to embrace updated phylogenetic pieces of information or knowledge about intraspecific variations along the rehabilitation trajectory.

7.8 Conclusion Eco-restoration of abandoned mine spoil sites and oil drilling sites have become an important part of the sustainable development strategy. Mine disposals and abandoned mines have caused air and water pollution through the dispersion of particles by wind and discharge of AMD water affecting aquatic life, human health, and change of entire landscape due to direct and indirect effect of mining/drilling. Physicochemical analysis of mine waste rocks and tailings show damaged topsoils and sandy structures with low fractions of clay, low/high pH values, high electrical conductivities, low amounts of soil nutrients, high concentrations of heavy metals, PAHs, and PCBs. The addition of FA serves multiple benefits for the reclamation of AMD sites in different ways like: (i) The alkaline nature of FA/CCP is ideal for fill or seal material of mining sites and can prevent the inception of AMD. The acidproducing materials in the mine spoil are neutralized by this alkaline amendment, (ii) A flowable fill seals and stabilizes abandoned underground mines to prevent subsidence and fights AMD, (iii) FA/CCP appears to be a good substrate for soil formation on abandoned mine lands where native soil is missing or damaged, (iv) Cost of mine site reclamation can be reduced significantly with the use of adequately available FA and this also solves storagerelated issues of FA to some extent, (v) Fly ash can cause the removal of many contaminants by precipitation, co-precipitation, and adsorption at the surface of the FA particles (Gitari et al., 2003). After treatment of mine sites with FA, vegetation cover on mine waste disposal is crucial to (i) prevent soil erosion by wind, (ii) stabilization of the steep slopes on the embankments of lagoons, (iii) decrease contaminants leaching in the groundwater and surroundings, (iv) addition of nutrients to the soil can enhance vegetation growth and amendments with some chelating compounds can bind contaminants and limit their mobilization and bioavailability, (v) establishment of native vegetation cover composed of grasses, legumes, shrubs/herbs and trees is a requisite for eco-restoration success. This speeds up the process of spontaneous colonization by numerous native tree species for permanent/long term stability and resilience of the ecosystem. Microbial processes or bioremediation should also go on along with

Phytoreclamation of abandoned acid mine drainage site  199 phytoremediation for enhancing mine spoil reclamation process and establishment of a stable nutrient cycle and return the damaged site to its original pristine condition that can survive as a self-sustaining ecosystem. Finally, including monitoring tools such as remote sensing and metabarcoding for understanding of ecorestoration success can boost our understandings about ecosystem functions such as nutrient cycling, establishment of biotic communities, and resource availabilities while providing solid information about the success of re-vegetation activities. A successful green phytocap on the mine site not only controls pollution, stabilizes the site, gives visual, and esthetic pleasure but harvesting of the bioenergy crops/trees and utilization of the biomass for biofuel creates alternative livelihood, reduces fossil fuel dependency, and prevents climate change.

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CHAPTE R 8

Chromium phytoaccumulation in lemongrass grown on chromium contaminated soil: Phytostabilization approach for chromium recovery from mining sites of Sukinda, India Deepak Kumar Patraa, Chinmay Pradhanb, and Hemanta Kumar Patrab a

Department of Botany, Nimapara Autonomous College, Nimapara, Puri, India bDepartment of Botany, Utkal University, Bhubaneswar, India

8.1 Introduction Phytoremediation is a green technology for the removal of toxic heavy metals from mining sites by using plants. Phytoremediation technology is commonly used to cover an extensive variety of plant-based eco-friendly techniques. Out of different techniques used for phytoremediation, phytoextraction involves the use of plants that accumulate metals via chelators in higher concentrations from the contaminated soil. During the phytostabilization process, the plants and microbes are exploited to decrease the soil leaching activity and help the removal of toxic metals from mine contaminated site. Lemongrass by its massive fibrous root system is a suitable material for the removal of heavy metals from contaminated soil by rhizofiltration technique, a technique that mostly involves the removal of pollutants from contaminated sites. Phytoremediation techniques are also helpful to enhance the degradation of contaminants and decrease the movement of toxic metals. In India, the state of Odisha accounts for about 98% of the total chromium deposit of the country. The South Kaliapani mining area of Sukinda (Odisha) alone contributes about 97% of the total chromite deposit of the state. The chromite ore is mostly processed by open cast mining activity releasing toxic hexavalent chromium (Cr+ 6) that contaminates the nearby biotic community and the river Brahmani. Currently around 14 chromite mines are operational in Sukinda valley. The huge open cast mining and industrial measures discharge a substantial amount of mine wastewater and effluents containing toxic metals at the operational sites causing environmental hazards. The huge quantity of particulate matter is also produced during the mining of chromite ore. The particulate matter from chromite Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00011-X © 2021 Elsevier Inc. All rights reserved.

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208  Chapter 8 mining encompasses the availability of Cr+ 6 which has a hostile effect on the environment. In addition, a large quantity of overburden soils is produced during open cast chromite mining process which is mostly rich in toxic chromium that contaminates the adjoining water, soil, and agricultural ecosystems. To withstand the severe problems of contamination of toxic hexavalent Cr ions from mine waste, the attempts have been made for lessening Cr load by phytoremediation effort using lemongrass. The studies on the reduction of chromium contamination levels in mine waste are being tested by using different plant categories (Landberg and Greger, 1996). The present issue is concerned with the phytoextraction of Cr from OBS of Sukinda mining site using lemongrass by different chelators and metal ions. This is basically based on chelate based phytoremediation technology. The chelators by phytoextraction process facilitate the availability of metals to plants (Salt et al., 1995) and thus, prevent soil contamination and promote phytostabilization activity. The chelators have been used successfully for induced phytoextraction as well (Salt et al., 1998). The intent of this experiment was to lessen the toxic impact of Cr in contaminated sites using lemongrass by chelators and metal ion supplementation.

8.2  Physicochemical properties of overburden soil The over burden soil (OBS) from South Kaliapani mining area of Sukinda were studied for their physicochemical and chromium contents. The OBS is a degraded one and contaminated with chromium of 92.5 mg/kg. The pH of the soil sample was 5.48. The acidic pH in heavy metals contaminated soil has also been observed by other workers (Lee et al., 2002). The values of electrical conductivity (EC) and cation exchange capacity (CEC) were 0.024 dS m− 1 and 12.65 meq/100 g, correspondingly. This might be accredited to the extreme quantity of chromium in the OBS. The calculated values of organic carbon (OC) and water holding capacity (WHC) of OBS were 1.92 g/kg and 37.0%. The available NPK and sulfur content were 164.0, 16.7, 21.0, and 2.70 in kg/ha, respectively. It has also been observed that the available Fe content of OBS was 2.05 mg/kg. The pH, EC, CEC, available NPK, and OC of OBS was increased with the addition of green manure and garden soil in 3:1 ratio in OBS.

8.3  Lemongrass for the restoration of mine soil of Sukinda The plants for phytostabilization of chromium in mining sites should be fast-growing, high soil binding fibrous root system, easily propagated, short life span, and high biomass. Lemongrass fulfills the above criteria. In addition, it is a fragrant plant and is cultivated mainly for oil production. The plants are not used for edible purposes and essential oil from the leaves is free from heavy metals accumulation (Zheljazkov et al., 2006). Due to its fragrance, the faunas do not consume it. The plants have well-developed root system and are quite helpful for the removal of chromium from mining sites (Patra et al., 2019). Lemongrass

Chromium phytoaccumulation in lemongrass  209 has been used as a model plant for assessment of chromium toxicity and phytostabilization of environmental chromium by the application of phytoremediation technology (Patra et al., 2019). For attenuation of chromium from OBS, pot experiments were carried out by the application of varied percentages of OBS and garden soil. (First treatment (T0)—Normal garden soil, Second treatment (T1)—300 g OBS + 2700 g garden soil, Third treatment (T2)— 600 g OBS + 2400 g garden soil, Fourth treatment (T3)—900 g OBS + 2100 g garden soil, Fifth treatment (T4)—1200 g OBS + 1800 g garden soil, Sixth treatment (T5)—1500 g OBS + 1500 g garden soil, Seventh treatment (T6)—2100 g OBS + 900 g garden soil, Eighth treatment (T7)— 3000 g OBS.) To increase the phytoextraction ability of lemongrass, the plantlets were treated with different type’s chelators such as ethylene diamine tetra acetic acid (EDTA), diethylene triamine penta acetic acid (DTPA), citric acid (CA), and salicylic acid (SA) and metals ions (Mg and Zn) in Cr-contaminated soil.

8.4  Plants response to chromium toxicity There was a decline in the growth of lemongrass plants when the plants were grown in varied concentrations (10%–100%) of OBS. The length and dry weight of the plants were not rigorously affected as other plants at T7 treatments in comparison to other treatments and control. The reduction in length and biomass of plants at T7 treatments (100% OBS) might be due to the toxicity of chromium. In the second and third treatments, the plants exhibited better growth (Figs. 8.1 and 8.2). It may be due to the availability of iron in the cellular level with the improvement of the structure of chloroplast at a lower concentration of chromium (Bonet et al., 1991; Erenoglu et al., 2007). The growth and development of roots were affected at a very high concentration of chromium available on OBS. As a result, the roots were unable to deliver the nutrients to shoot, for which the plant development was affected. Similar results were observed by other workers (Patra et al., 2018a). The inhibition of growth of root is a

Fig. 8.1 Effect of Cr on root and shoot length of lemongrass plants.

210  Chapter 8 30

Root fr. wt.

Shoot fr. wt.

Root dry wt.

Shoot dry wt.

Weight (g)

25 20 15 10 5 0 T0

T1

T2

T3

T4

T5

T6

T7

Soil treatments

Fig. 8.2 Effect of Cr fresh and dry weight of root and shoot of lemongrass plants.

prime symptoms of metal toxicity and this symptom is the best indicator to determine the level of lenience (Wong and Bradshaw, 1982). The total chlorophyll and protein contents marginally decreased at a higher concentration of chromium treatments (T7). The amount of chlorophyll pigments depends upon the concentration of Fe. Although iron is not a constituent of the chlorophyll molecule, but it is essential for its formation. The excessive application of chromium blocks the entry of Fe in to the site of chlorophyll synthesis due to competitive inhibition and thus, resulted in the decline of chlorophyll biosynthesis (Brown, 1956). The decrease in protein amount with enhancing the level of chromium might be due to the breakdown of proteins by protein degrading enzymes (Romero-Puertas et al., 2002). But the chlorophyll and protein contents increased in other treated plants, in contrast, to control (Fig. 8.3). The amino acid proline accumulated to a large extent in treated plants in comparison to control (T0). Proline accumulation is a key stress indicator to assess the oxidative stress impact on plants (Mohannty et al., 2011). The application of chromium augmented the activity of antioxidant enzymes (Fig. 8.4). But the activity of peroxidase was more in plants than catalase. It was observed that the chromium present in OBS induces oxidative stress by producing reactive oxygen species (ROS) in plants that stimulate the activity of enzymes, which constrains the reactions endorsed by the ROS (Patra et al., 2019). The accumulation of ROS in plants is a feature of stress induction. The ROS increased with an increase in the concentration of chromium in OBS (Fig. 8.5). The excessive production of ROS occurred in T8 treatment. Further, it was noticed that ROS increased the lipid peroxides in tissues of lemongrass plants (Fig. 8.6). At a very high concentration of chromium, the growth of plants was affected because the defense system of the plants fails to scavenge the ROS due to the lessening of proline level and activity of oxidative inhibitors enzymes.

Chromium phytoaccumulation in lemongrass  211

Fig. 8.3 Effect of Cr on total chlorophyll, protein, and proline of lemongrass plants. 90

Leaves (CAT) Leaves (SOD) Leaves (POX)

Roots (CAT) Roots (SOD) Roots (POX)

80

Activity (unit/g fr. wt.)

70 60 50 40 30 20 10 0 T0

T1

T2

T3

T4

T5

T6

T7

Soil treatments

Fig. 8.4 Effect of Cr on the changes of catalase, peroxidase, and superoxide dismutase activity (unit/g fresh wt.) of lemongrass plants.

The oil of lemongrass is economically significant and its quality is based on citral-a and production. The quality and quantity of oil in the lemongrass plant gradually increased with an increase in the concentration of Chromium up to T6 treatments. The reduction of oil and citral contents of lemongrass plants decreased at T7 treatments (Table 8.1). The accumulation of Cr gradually upsurged in plant roots and shoots through a rise in the application of Cr (Fig. 8.7). Similar observations were reported earlier (Zhang et al., 2007). The maximum chromium accumulation was observed in roots and shoots with the application

Fig. 8.5 Effect of Cr on the production of reactive oxygen species of lemongrass plants. 100

TBARS (nmol/g fr.wt.)

90

Lipid peroxidation

80 70 60 50 40 30 20 10 0

T0

T1

T2

T3

T4

T5

T6

Soil treatments

Fig. 8.6 Effect of Cr on lipid peroxidation of lemongrass plants. Table 8.1: A comparison between total Cr ­concentration in garden soil, overburden soil, and different mixture. Treatments T0 T1 T2 T3 T4 T5 T6 T7

Total Cr contents (mg/kg) 0 9.25 18.5 27.75 37.0 46.25 64.75 92.5

T7

Chromium phytoaccumulation in lemongrass  213 45 Root

Total Cr (mg/g dry wt.)

40

Shoot

35 30 25 20 15 10 5 0 T0

T1

T2

T3 T4 Soil treatments

T5

T6

T7

Fig. 8.7 Effect of Cr on total chromium content of root and shoot of lemongrass plants. Table 8.2: Essential oil content and a major constituent of lemongrass. Treatments T0 T1 T2 T3 T4 T5 T6 T7

Oil content (%) (mean ± SE) 0.4 ± 0.05 0.72 ± 0.005 0.75 ± 0.005 0.5 ± 0.057 0.4 ± 0.057 0.5 ± 0.057 0.6 ± 0.057 0.5 ± 0.057

Citral content (%) (mean ± SE) RI (citral a/b) 14.99/15.89 15.87/16.5 15.99/16.8 15.89/16.4 17.05/18.33 17.05/18.32 17.32/18.45 16.82/17.87

Citral-a

Citral-b

35.47 ± 0.005 55.26 ± 0.005 55.23 ± 0.005 55.94 ± 0.005 56.11 ± 0.005 57.99 ± 0.038 59.81 ± 0.005 55.99 ± 0.005

24.41 ± 0.1005 26.06 ± 0.005 26.09 ± 0.005 26.44 ± 0.005 27.84 ± 0.005 28.78 ± 0.005 24.15 ± 0.005 26.37 ± 0.005

of 100% OBS. The total accumulation rate (TAR), transportation index (Ti) increased with an increase in the concentration of chromium. On the other hand, bio-concentration factor (BCF) and tolerance index (TOI) values decreased with the application of a higher concentration of chromium (Table 8.2). The maximum Ti value for Cr was observed in T4 while maximum TAR in T2.

8.5  Chelate and metal-assisted phytoextraction of chromium from overburden soil The physicochemical properties of OBS were improved by the addition of chelators and metals ions. Patra and his co-workers (2018c) also reported that the applications of chelating agents increased the EC, CEC, and WHC of soil. In chelate assisted OBS the value of available Cr content was very less which was due to uptake of Cr by lemongrass plants. The applications of chelators were based on ideas for improving heavy metal uptake in plants and restraining the discharge of heavy metals from contaminated soil.

214  Chapter 8 There was an enhancement of plant growth in OBS treatments without chelators (T1) as compared to control. There was promotional growth of lemongrass plants due to applications of chelators, Mg, and Zn to T1 treatments. However, the applications of DTPA, citric acid, Mg, and Zn were found more effective on plant growth as compared to other chelators. The applications of chelating agents have been shown to improve the solubility and uptake of nutrients in plants. The use of chelating agents such as EDTA, DTPA, citric acid, salicylic acid, etc. are known to enhance the availability of metals to the plants by uptake mechanisms (Turanu, 1998). The applications of chelators and metal ions to OBS were advantageous for the stimulation of plant growth. In addition, there was also a reduction in the levels of chromium in contaminated soil. The chlorophyll and protein contents increased further in leaves of lemongrass when grown in Cr-contaminated OBS assisted by different chelators and metal ions like Mg and Zn. At the same time, a noticeable rise in proline amount was also observed in leaves when Crcontaminated OBS were assisted by the chelators (DTPA and CA) and metal ions (Mg+ 2). The total chromium at root and shoot is positively correlated with total chlorophyll and protein (P-value  Ni2  + > Co2  + > Mn2  + > Zn2  +. Depending on the mineral structure, this process may occur within or on the surface of the plant (Fijalkowski et al., 2012; Gang et al., 2010). Soil organic matter is generally identified as having a dominant role in influencing trace metal behavior in soil (Laghlimi et al., 2015; Sherene, 2010). Plant absorption of heavy

Gold mining industry influence on the environment  385 metals is reduced by increasing the quantity of soil organic matter. The presence of organic carbon enhances the soil’s cation exchange capability, which retains plant-assimilated nutrients (Laghlimi et al., 2015). Plant-related factors involve plant root depth and density, transpiration rate, root absorption factor, rhizosphere acidification, rhizosphere exudates and secretions, and environmental conditions regulating the metals translocation from root to the surface (Kidd et al., 2009; Sheoran et al., 2016). The potential quantity of metal absorbed by the plant roots and the root density of the plant varies depending on depth. Most plant roots are found near the surface of the soil, and the root density reduces as the depth increases. Therefore, the selected plants must have roots growing at an adequate depth that are able of entering the soil solution (Sheoran et al., 2016). The process of uptake of soil solution from the roots and translocation to the green parts of the plant is called transpiration. The rate of transpiration is climate-dependent; however, higher concentrations of metal in the plant roots can be a consequence of water uptake by the plant, which induces metal migration via mass flow to the root surface area, where precipitation occurs (Sheoran et al., 2016). The metal must enter the root before its translocation to the aerial sections of a plant, either through the symplastic or apoplastic pathways where active and passive filters can manifest (Marschner, 1995). Rhizobiological activity, temperature, pH, moisture, root exudate, the competing ions concentration, and the presence of metals, also influences the root absorption factor (Sheoran et al., 2016). The root proton (H+) secretion is performed by plasma membrane H+-translocating adenosine triphosphatase and other H+ pumps, acidifies the rhizosphere area, and enhances the dissolution of metals (Ghosh and Singh, 2005). Numerous hyperaccumulator plant roots exude organic acids and reduce pH in the rhizosphere, causing bioavailability of metal cations (Ross, 1994).

16.4.3  Heavy metal phytotoxicity Phytotoxicity has generally been connected with a phenomenon through which a possibly hazardous element has accumulated in plant tissue at a degree that has an impact on optimal growth and plant development (Baker, 1987; Beckett and Davis, 1977; Naidu et al., 2003). The toxic effects of heavy metals in the soils may not vary based on their abundance but the bioavailable fraction, that can be adjusted through rhizosphere processes or the introduction of specific additives (Ernst, 1996; Mench et al., 1994).

386  Chapter 16 Heavy metals phytotoxicity results from the imbalance between the absorption of the element and the inability of the metabolism to accommodate with its cellular concentration, in particular, cytosolic concentration. Surplus heavy metals on plant tissues trigger a series of phytotoxic effects and metabolic processes, depending on the metal-specific reaction pattern. The toxic effects of heavy metals first affect the root and the root plasma membrane. Once the excess amount of free metals accumulates in the cytoplasm, it will deregulate the cell metabolism by interfering with the protein reactions center and by inducing the development of stress peptides, such as stress proteins and phytochelatins. If soil acidification is further enhanced, the bioavailable heavy metals fraction in soils will, therefore, raise the risk for plant damage due to the excess of heavy metals (Ernst, 1996). Gold mine tailings contain high levels of toxic metals such as Cu, Pb, Zn, Cd, As, and Hg with negative influence on plants. Several plants and bacteria have developed tolerance to the excess of Cu. Plants growing on Cu-polluted sites appear to accumulate elevated concentrations of Cu, notably in the vicinity of industrial areas (Fishelson et al., 1994; Kabata, 2011; Reimann et al., 1999). The Cu phytotoxicity is depending on the distribution of different chemical forms and soil characteristics, including soil pH and organic matter content (Alva et al., 2000). Pb has a negative impact on plant photosynthesis, seed germination, seedling growth, plant water status, root and shoot dry mass, enzymatic activities, and mineral nutrition (Munzuroglu and Geckil, 2002; Pinho and Ladeiro, 2012). Although, Zn is not considered to be highly phytotoxic, in many soils it has reached phytotoxic concentrations due to the contamination by anthropic activities (Chaney, 1993). Zn phytotoxicity is frequently observed in acidic and heavily sludge soils. The toxicity level of Zn is depending on the species of plants and genotypes, and also on the growth stage (Kabata, 2011). Cd is one of the most toxic environmental pollutants and has been widely spread to the environment as a consequence of mining and other industrial uses, Cd plant contamination being a major environmental issue (Jaskulak and Grobelak, 2019). Cd phytotoxicity mechanisms impede metabolic processes including photosynthesis, respiration, gas exchange, and water relations, and may also concentrate in chloroplasts (Balen et al., 2011; Dong et al., 2006; Jaskulak and Grobelak, 2019). As phytotoxicity depends on its chemical speciation and availability, arsenite being more toxic than arsenate. Arsenite reacts with enzyme and protein groups of sulfhydryl which impact plant metabolism (Manzano et al., 2016). The As toxicity was widely observed in plants growing in soils contaminated with mine waste. As toxicity symptoms are identified as slowing in development, wilting of the leaves, violet pigmentation, root discoloration, and plasmolysis of the cells (Kabata, 2011).

Gold mining industry influence on the environment  387 Plant exposure to Hg has an impact on the antioxidant defense system, has been associated with seed injuries, and reduces seed viability, photosynthesis, chlorophyll synthesis, transpiration, and water uptake (Azevedo and Rodriguez, 2012).

16.5  Phytoremediation strategies/technologies Phytoremediation can be described as an emerging technology that uses the bioaccumulation capacities of specialized groups of green plants for cleaning up the environment by relief, transfer, stabilization, or depletion of heavy metals and metalloids from the soil, sediments, surface waters, and groundwater. Various associations and interactions between plants, their microbial rhizosphere flora, and pollutants make these multiple phytoremediation mechanisms practical for a variety of organic and inorganic contaminants. Some plant roots possess the ability to absorb and immobilize metal contaminants, while other species can metabolize or retain chemical and nutrient contaminants (Laghlimi et al., 2015; Pilon-Smits, 2005; Purakayastha and Chhonkar, 2010; Sarwar et al., 2017). Phytoremediation is not a new concept; approximately 300 years ago, several plants were suggested for wastewater treatment (Hartman Jr., 1975; Purakayastha and Chhonkar, 2010). The first reported plant species that accumulate great amounts of metals in their leaves are Viola calaminaria and Thlaspi caerulescens (Baumann, 1885). Phytoremediation is considered to be more efficacious compared to traditional techniques due to the added benefits provided by the plants (Chakravarty et al., 2017).

16.5.1 Phytostabilization Phytostabilization is described as (1) soil metal immobilization by root absorption and accumulation, root adsorption, or precipitation within the root zone and (2) plants and plant roots utilization to avoid pollutant propagation through water erosion and wind, soil dispersion, and leaching (EPA, 2000; Hasanuzzaman and Fujita, 2013). Phytostabilization takes place through root-zone chemistry and microbiology and soil or contaminant chemistry alteration (EPA, 2000) via precipitation, sorption, complexation, or reduction of metal valence (Hasanuzzaman and Fujita, 2013). This technology is an indirect remediation method of metal pollution, being very efficient for the rapid immobilization of contaminants, preventing their migration into soil and surface water (Saxena and Misra, 2010). This approach can be used to restore the vegetation cover at sites where there is a loss of natural vegetation due to high metal concentrations in surface soils (Miller, 1996; Salt et al., 1995).

388  Chapter 16 16.5.1.1  Advantages and limitations of phytostabilization Phytostabilization has several advantages as follows: the soil removal is not necessary; it is cost-efficient than other technologies; ecosystem restoration is enhanced by revegetation, and the disposal of hazardous materials or biomass is not mandatory. One of the significant issues of this method is that the contaminants are not extracted; they remain in the ground and may demand ongoing maintenance to avoid their rerelease and potential leaching. Besides, the root region, root exudates, pollutants, and soil changes must be constantly monitored to avoid metal solubility and leaching from augmenting. Consequently, the field will remain polluted and unsuitable for agriculture. Other disadvantages are that plants may require substantial fertilization or soil modification through amendments and metals plant uptake and translocation to the aboveground section should be prevented (EPA, 2000). 16.5.1.2  Plants used in phytostabilization Brassica juncea can decrease metals leaching from the soil by more than 98% (Raskin et al., 1994; EPA, 2000). For the phytostabilization of soils contaminated with Zn, Pb, and Cu, Festuca rubra and Agrostis tenuis are used (Cioica et al., 2019; Galende et al., 2014; Hasanuzzaman and Fujita, 2013; Smith and Bradshaw 1992). Cd forms compounds with sulfides in the rhizosphere region of the Agrostis capillaris and Silene vulgaris species, and Pb is transformed into an insoluble component (phosphate) which supports them as phytostabilizer of land polluted with these heavy metals (Cioica et al., 2019; Khalid et al., 2017; Vasavi et al., 2010). According to Salt et al., 1995, some species of grasses have been used to mitigate metal leaching: Colonial bentgrass (A. tenuis cv Parys) has been used for Cu mine waste; Colonial bentgrass (A. tenuis cv Goginan) was used for acid Pb and Zn mine waste; Red fescue (F. rubra cv Merlin) has been used for calcareous and Zn mine waste (EPA, 2000). Medicinal and aromatic plants, such as Melissa officinalis L., Ocimum basilicum L., Valeriana officinalis L., Matricaria chamomilla L., and Calendula officinalis L. are recommended for phytostabilization of soils polluted with Pb, Zn, and Cd (Achakzai et al., 2011; Cioica et al., 2019; Masarovicova et al., 2010).

16.5.2 Phytoextraction Phytoextraction (also called phytoaccumulation or phytomining) is the most significant method of phytoremediation for the elimination of metals and metalloids from polluted soil, water, biosolids, and sediments, using nonfood crops. This technique is based on the

Gold mining industry influence on the environment  389 absorption of contaminants by the roots of the plant and their translocation and transport to harvestable plant biomass (EPA, 2000; Hasanuzzaman and Fujita, 2013; Laghlimi et al., 2015; Sarwar et al., 2017). Phytoextraction is predominantly used in soil, sediments, and sludge recovery and, to a lesser extent, in the treatment of contaminated water (EPA, 2000). The application of phytoextraction requires the cultivation of hyperaccumulators, plants with the ability to tolerate and accumulate substantial quantities of heavy metals in their tissues. More than 45 plant families have been reported as hyperaccumulators, including Brassicaceae, Euphorbiaceae, Fabaceae, Asteraceae, Scrophulariaceae, and Lamiaceae (Baker et al., 1994; Hasanuzzaman and Fujita, 2013; Salt et al., 1998). Various phytoextraction techniques have been researched, but literature focuses mostly on two essential approaches: continuous or induced phytoextraction. Continuous phytoextraction (natural hyperaccumulation) is used for the elimination of pollutants based on the plant’s natural ability to remediate or remove contaminants from the polluted environment. Induced/ chelated-assisted phytoextraction (induced/assisted hyperaccumulation) implies the addition of conditioning agents (oligopeptide ligands) containing artificial chelates or other acidifying agents to enhance the mobility and efficient uptake by the plant that is going to be used for heavy metal contaminants phytoremediation (Erakhrumen, 2013; Salt et al., 1995, 1998). Among plant species exposed to heavy metals, about 100 phytochelatin ligands have been identified (Rauser, 1999). 16.5.2.1  Advantages and limitations of phytoextraction The effectiveness of phytoextraction depends, in particular, on high metal uptake and translocation accumulation ability, resistance to high metal concentrations without toxic symptoms, high biomass production capacity, rapid growth patterns, and a broad root system of the plants to be used (Blaylock et al., 1997; Blaylock and Huang, 2000; Hasanuzzaman and Fujita, 2013; McGrath, 1998). It also required the capacity of plants to tolerate challenging soil conditions (e.g., pH, salinity, water content, soil composition) (Hasanuzzaman and Fujita, 2013; Jabeen et al., 2009). The disadvantage of the phytoextraction method is attributed to the limitation of the extraction of toxic metals to shallow soil depths (61 cm) and to some characteristics of hyperaccumulators, that are mostly slow-growing, low-biomass-producing species, and lacking useful agronomic features (Cunningham et al., 1995; Hasanuzzaman and Fujita, 2013). 16.5.2.2  Plants used in phytoextraction Alpine Pennycress (T. caerulescens L.), effective in Zn2  +, Cd2  +, and Ni2  + hyperaccumulation (Milner and Kochian, 2008), Indian mustard (B. juncea), Serpentine endemic shrub

390  Chapter 16 (Alyssum sp.), and Astragalus racemosus are the most known natural hyperaccumulators (Chatterjee et al., 2013). B. juncea (Indian mustard) can accumulate Cd, Pb, Cu, Cr(VI), Zn, Ni, B, 90Sr, and Se (EPA, 2000; Nanda Kumar et al., 1995; Raskin et al., 1994; Salt et al., 1995). It has the uppermost capacity to transport Pb to shoots, accumulating more than 1.8% Pb in the shoots, its concentration ranging between 0.04%–3.5% in the shoots and 7%–19% in the roots (EPA, 2000; Nanda Kumar et al., 1995).

16.5.3 Phytovolatilization Phytovolatilization is a distinct method of phytoremediation involving the plants to accumulate soil contaminants, preceded by transformation into modified volatile forms of the contaminants and release into the atmosphere through transpiration, by the foliar system (EPA, 2000; Ghosh and Singh, 2005; Salt et al., 1998; Sarwar et al., 2017). This technique is mainly useful for Hg and Se, along with As, in which metals are transformed into volatile forms for release and dilution into the atmosphere through transpiration (Bhargava et al., 2012; Chatterjee et al., 2013; EPA, 2000). 16.5.3.1  Advantages and limitations of phytovolatilization The main advantage of this method is that contaminants are transformed into less toxic forms. The mercuric ion is changed into less toxic elemental mercury and selenium in dimethyl selenite gas (Chatterjee et al., 2013; EPA, 2000). The disadvantage of this method is that the contaminants might accumulate in vegetation and metabolites can be transported to the upper parts of the plants and found in fruits (EPA, 2000; Newman et al., 1997) 16.5.3.2  Plants used in phytovolatilization Plants can remove Methyl-Hg from contaminated soil by introducing bacterial merA and merB genes into numerous species of plants, including Arabidopsis, poplar, tobacco, cottonwood, and rice (Bizily et al., 2000; Chatterjee et al., 2013; Czako et al., 2006; Heaton et al., 2003; Lyyra et al., 2007; Rugh et al., 1996). Various plants, such as transgenic A. thaliana (Rugh et al., 1996; Yang et al., 2003), Oryza sativa (Heaton et al., 2003), Nicotiana tabacum (Chatterjee et al., 2013; Ruiz et al., 2003), Liriodendron tulipifera (Rugh et al., 1998), become more Hg2  + and R-Hg+ tolerant and release 10 times more elemental Hg in comparison to nontransformed plants (Chatterjee et al., 2013). Selenium is toxic in most plant species following metabolization into amino acid cysteine and methionine analogs. A specific enzyme found in selenium hyperaccumulating plant species

Gold mining industry influence on the environment  391 (selenocysteine methyltransferase) is responsible for transforming selenate into methyl selenocysteine, which is eventually incorporated into the proteins and hyperaccumulates selenium. Selenite can also be metabolized to dimethyl selenide, a 100 times less damaging component (Chatterjee et al., 2013; Terry et al., 2000). Transgenic Indian mustard (B. juncea L.) transmuted with the selenocysteine methyltransferase gene from Se-hyperaccumulator Astragalus bisulcatus produces significantly higher dimethyl selenide along with the amplified Se-accumulation and level of tolerance, compared to control plants (Chatterjee et al., 2013; LeDuc et al., 2004). Canola (B. napus) and Indian mustard (B. juncea) have been used for Se phytovolatilization (Adler 1996). Tall fescue (Festuca arundinacea Schreb cv. Alta) and kenaf (Hibiscus cannabinus L. cv. Indian) were also used but to a smaller extent than canola (Bañuelos et al., 2005; EPA, 2000).

16.5.4 Rhizofiltration Rhizofiltration, also referred to as phytofiltration, is a phytoremediation mechanism that uses terrestrial and aquatic vegetation to uptake, accumulate, and precipitate metals from polluted sources via the root system (Ghosh and Singh, 2005). This technique is successful in extracting poisonous metals from aquatic environments such as groundwater and damp soils by the rhizosphere (Hasanuzzaman and Fujita, 2013). Rhizofiltration can be used for heavy metals removal, such as Cu, Cd, Pb, Zn, Ni, and Cr, principally retained inside the roots of the plants (Chaudhry et al., 1998; Hasanuzzaman and Fujita, 2013; Saxena and Misra, 2010; USEPA, 2000). A suitable rhizofiltration plant should have an extensive root system under which the poisonous metals are absorbed from the solution (Chatterjee et al., 2013). 16.5.4.1  Advantages and limitations of rhizofiltration Rhizofiltration has the advantage of using both terrestrial and aquatic plants. While terrestrial plants necessitate support, like floating platforms, they typically extract more contaminants than aquatic plants. This structure can be placed in situ (floating rafts on ponds) or ex situ (an engineered tanks system) (EPA, 2000). It reported that aquatic plants have limited potential in rhizofiltration processes due to their small, slow-growing roots, and high-water content, which makes their drying, composting, or incineration complicated (Dushenkov et al., 1995). Also, to obtain maximum metal absorption, the pH of the influential solution may need to be continuously adjusted. Another disadvantage is that the plants (particularly terrestrial plants) may need to be first cultivated in a greenhouse and then installed in the rhizofiltration system (EPA, 2000).

392  Chapter 16 16.5.4.2  Plants used in rhizofiltration A variety of plants, such as Indian mustard (B. juncea), corn (Zea mays), and sunflower (Helianthus annuus) are suitable plants for rhizofiltration (Brooks and Robinson, 1998; Chatterjee et al., 2013). Many aquatic plant species have been reported with the ability to extract heavy metals from water, such as pennywort (Hydrocotyle umbellata), water hyacinth (Eichhornia crassipes), and duckweed (Lemna minor) (Dierberg et al., 1987; Hasanuzzaman and Fujita, 2013; Mo et al., 1989; Setia et al., 2008; Zhu et al., 1999). Water hyacinth (E. crassipes) efficiently extracts trace elements from waste streams (Hasanuzzaman and Fujita, 2013; Zhu et al., 1999).

16.5.5 Phytostimulation Phytostimulation is also known as rhizodegradation, rhizospheric biodegradation, plantassisted bioremediation/degradation, or enhanced rhizosphere biodegradation (EPA, 2000; Hasanuzzaman and Fujita, 2013). It involves the breakdown of soil contaminants through the rhizosphere microbial activity (Chatterjee et al., 2013; Saxena and Misra, 2010), depending on plant secretions in root exudates that sustain the growth and metabolic processes of various bacterial and fungal species in the rhizosphere, being capable of degrading diverse contaminants (Anderson et al., 1993; Hasanuzzaman and Fujita, 2013). Due to the presence of these exudates, which include carbohydrates, organic acids, amino acids, fatty acids, sterols, nucleotides, growth factors, enzymes, flavanones, and other compounds, the microbial activity in the rhizosphere may be enhanced (EPA, 2000; Schnoor et al., 1995; Shimp et al., 1993). This method is used to decontaminate organic pollutants; microorganisms, including bacteria, fungi, and yeast, absorb and assimilate solvents and fuels (Ghosh and Singh 2005; Hasanuzzaman and Fujita, 2013). In situ destruction of pollutants and the lack of their translocation to the plant or atmosphere are the main advantages of phytostimulation. The disadvantages of this method are related to the limitation of the root depth due to the soil’s physical structure or moisture conditions, and the extensive time required for the development of the roots. Also, plants might need additional fertilization due to the microbial nutrient competition, and exudates may stimulate nondegrading microorganisms to the detriment of degraders (EPA, 2000).

16.5.6 Phytodegradation Phytodegradation is also recognized as phytotransformation and discusses the uptake of organic pollutants by plants themselves, through numerous internal enzymatic reactions and metabolic processes through subsequent breakdown, metabolization, or mineralization (Salt et al., 1998; Spaczynski et al., 2012). As a consequence of primary and secondary

Gold mining industry influence on the environment  393 metabolism, plants synthesize a significant number of enzymes and can efficiently uptake and metabolize organic pollutants into less toxic complexes (Hasanuzzaman and Fujita, 2013). The main advantage of this method is that contaminant degradation due to plant-produced enzymes can occur in a microorganism-free environment, but toxic and degradation products may develop. Removal of pollutants could be difficult to confirm as the presence and nature of metabolites within a plant may be difficult to determine (EPA, 2000).

16.6  Phytoremediation applications Phytoremediation of numerous inorganic contaminants (Cu, Pb, Zn, Cd, As, etc.) has been intensively investigated. This process is focused on the use of natural hyperaccumulator plants with an excellent metal-accumulating capacity, and the ability to tolerate high concentrations of hazardous metals than the typical plants. The discovery of plants’ metal-accumulating properties contributed to the progress of phytoremediation technologies. Over 400 varieties of hyperaccumulator plants currently exist for inorganic contaminants (Mahmoud and Hamza, 2017).

16.6.1  Plant selection considerations The nature of on-site pollutants is a significant factor in the selection of a phytoremediation plant (Laghlimi et al., 2015; Sharma and Reddy, 2004). Plants used for phytoremediation tasks should be chosen based on several features of the plants. Besides, important environmental considerations for selecting the best remediation solution include soil type and representative parameters (pH, salinity, average humidity, metal content, nutrient content), depth of contamination, the presence of pathogens, altitude, and the estimated volume of precipitation during the remediation process are the key factors (Fellet et al., 2013; Hasanuzzaman and Fujita, 2013; Kvesitadze et al., 2006). The plant species used for phytoremediation are carefully chosen based on their root depth. The depth of the plant root directly influences the soil depth that can be phytoremediated (Laghlimi et al., 2015). The remediation depths are almost less than 3 ft for grasses, less than 10 ft for shrubs, and less than 20 ft for deep rooting trees (Laghlimi et al., 2015; Sharma and Reddy, 2004). The phytoremediation efficiency of a plant depends on the metal volume that can be accumulated without plant toxic symptoms and on its ability to transform such heavy metals through systematic cell metabolism (Hasanuzzaman and Fujita, 2013; Kvesitadze et al., 2006). Intensely evaluated herbaceous plants, particularly grasses, have been more recommended for phytoremediation because, in contrast to trees and shrubs, they have features of rapid growth,

394  Chapter 16 high amounts of biomass, significant resistance, efficient soil stabilization, and the ability to phytoremediate different soil types (Elekes, 2014; Laghlimi et al., 2015). Their fibrous roots and extensive soil penetration prevent leaching, drainage, and soil erosion by stabilization and provide advantages for phytoremediation (Garba et al., 2012). Grasses, may easily create aboveground closures and reduce tailings dust dispersion (Hamzah and Priyadarshini, 2014). To attain a stable permanent cover, it is necessary to use a mixed crop and to associate trees, shrubs, and grasses, and in the mining soil revegetation program as they constitute useful plants types with distinct roles in the improvement and recovery of mine soils (Laghlimi et al., 2015). Brassicaceae family contains numerous metal-accumulating plants and has gained much recognition as several hyperaccumulators belong to this family of plants (Broadley et al. 2001; Fellet et al., 2013; Krämer, 2010).

16.6.2  Heavy metals phytoremediation: Cu, Pb, Zn, Cd, As, and Hg Worldwide scientists have been working since the early 1990s to apply selected hyperaccumulative species of plants to phyto-extract metals and semimetals from contaminated soils (Brown et al., 1994; Brooks and Robinson, 1998; Chaney et al., 2007; Rascio and Navari-Izzo, 2011). For hyperaccumulation, the minimum metal content (dry mass related) is 1% for Ni, Zn, and Mn; 0.1% for As, Cu, Pb, Se, and Co; and 0.01% for Cd (Brooks and Robinson, 1998; Karczewska et al., 2015). Due to its large biomass, sunflowers are useful for the phytoremediation of soils with metal contamination. Nehnevajova et al. (2005) identified that the “Salut” cultivar showed increased cumulative efficiencies in Zn, Pb, and Cd extraction (Purakayastha and Chhonkar, 2010). Table 16.1 summarize the most tested plant species that showed potential for the phytoremediation of the main contaminants related to gold mining (Cu, Pb, Zn, As, Cd). Copper: There are almost 40 species in the plant group recognized as Cu and Co hyperaccumulators (Table 16.1), including Haumaniastrum katangense (Lamiaceae) (Brooks and Robinson, 1998; Karczewska et al., 2015). Elsholtzia splendens has recently been established as tolerant to high concentrations of Cu and has significant potential to remediate polluted soils (Jiang et al., 2004; Purakayastha and Chhonkar, 2010; Wu et al., 2007). Milyang 23 rice and Gold Dent maize from low to moderately polluted paddy soils, under aerobic soil settings, have great potential for Cu phytoextraction (Murakami and Ae, 2009; Purakayastha and Chhonkar, 2010). Lead: Indian mustard (B. juncea) is broadly reported as a good Pb hyperaccumulator, and Pb accumulation in roots was nearly 10 times higher than in shoots (Table 16.1). Several other plants are described with high Pb-accumulating features, such as common ragweed

Gold mining industry influence on the environment  395 Table 16.1: Plant species with phytoremediation potential for main gold mining contaminants. Contaminant Cu

Possible hyperaccumulator plants

Reference

Aeolanthus biformifolius Brassica juncea

Morrison et al. (1979) Bennett et al. (2003), Ebbs and Kochain (1997), Inoue et al. (2003), and Purakayastha et al. (2008) Jiang et al. (2004), Wu et al. (2007), and Xiao et al. (2005) McCutcheon and Schnoor (2003) Baker and Walker (1990) McCutcheon and Schnoor (2003) Videa-Peralta (2002) Kim et al. (2003) Vamerali et al. (2009) Vamerali et al. (2009) Boyd and Davis (2001) Inoue et al. (2003) Berti and Cunningham (1993) Berti and Cunningham (1993) Evangelou et al. (2007) Bennett et al. (2003), Begonia et al. (1998), Blaylock et al. (1997), and Huang et al. (1997) Berti and Cunningham (1993) Berti and Cunningham (1993) Lai and Chen (2004) Krishnasamy et al. (2004) Paz-Alberto et al. (2007) Paz-Alberto et al. (2007) Evangelou et al. (2007) Huang et al. (1997) Vamerali et al. (2009) Vamerali et al. (2009) Evangelou et al. (2007) Surat et al. (2008) Robinson et al. (1998) Baker and Walker (1990) Gupta et al. (2008), Lai and Chen (2004), Paz-Alberto et al. (2007), and Wilde et al. (2005) French et al., 2006) Cosio et al. (2004), Kupper et al. (2000), Sarret et al. (2002), and Zhao et al. (2000) Bennett et al. (2003), Ebbs et al. (1997), Kumar et al. (1995), and Salt et al. (1995) Lai and Chen (2004)

Elsholtzia splendens

Pb

Haumaniastrum robertii Ipomoea alpine Larrea tridentata Medicago sativa Polygonum thunbergii Populus sp. Salix sp. Streptanthus polygaloides Zea mays Ambrosia artemisiifolia Apocynum cannabinum Borago officinalis Brassica juncea

Carduus nutans Commelina communis Dianthus chinensis Fioria vitifolia Imperata cylindrica L. Paspalum conjugatum L. Phacelia boratus Pisum sativum Populus sp. Salix sp. Sinapis alba L. Sonchus arvensis Thlaspi caerulescens Thlaspi rotundifolium Vetiveria zizanioides

Zn

Alnus sp. Arabidopsis halleri

Brassica juncea

Dianthus chinensis

Continued

396  Chapter 16 Table 16.1  Plant species with phytoremediation potential for main gold mining contaminants—cont’d Contaminant

Possible hyperaccumulator plants

Reference

Pennisetum americanum, P. atratum Polygonum thunbergii Populus sp.

Zhang et al. (2010) Kim et al. (2003) French et al. (2006) and Vamerali et al. (2009) Qiu et al., (1997) French et al. (2006) and Vamerali et al. (2009) Boyd and Davis (2001) Brown et al. (1994, 1995), Chaney (1983), Ernst (1968, Escarre et al. (2000), Frey et al. (2000), and Cosio et al. (2004) Lai and Chen (2004) Mahmud et al. (2008) Gisbert et al. (2008) and Mahmud et al. (2008) Mahmud et al. (2008) Gisbert et al. (2008) Gisbert et al. (2008) Ampiah-Bonney et al. (2007) Ampiah-Bonney et al. (2007) Mahmud et al. (2008) Francesconi et al. (2002) Vamerali et al. (2009) Wang et al. (2006) Ampiah-Bonney et al. (2007), Gonzaga et al. (2008), Ma et al. (2001), Tu and Ma (2002), and Tu et al. (2002) Vamerali et al. (2009) Gisbert et al. (2008) Mahmud et al. (2008) Videa-Peralta (2002) Greger (1999) Li et al. (2009) Evangelou et al. (2007) Ebbs and Kochain (1997), Ghosh and Singh (2005), Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Ghosh and Singh (2005) Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000)

Potentilla griffithii Salix sp. Streptanthus polygaloides Thlaspi caerulescens

As

Vetiveria zizanioides Azolla pinnata Bassia scoparia Eichhornia crassipes Hirschfeldia incana Inula viscosa Leersia oryzoides Lemna gibba L. Monochoria vaginalis Pityrogramma calomelanos Populus sp. Pteris multifida, P. oshimensis Pteris vittata

Cd

Salix sp. Solanum nigrum Spirodela polyrhiza Alfalfa Alyssum murale Averrhoa carambola Borago officinalis Brassica juncea, B. napus

Datura innoxia Gossypium hirsutum

Gold mining industry influence on the environment  397 Table 16.1  Plant species with phytoremediation potential for main gold mining contaminants—cont’d Contaminant

Possible hyperaccumulator plants

Reference

Helianthus annuus

Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Ghosh and Singh (2005) Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Videa-Peralta (2002) Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Griga et al. (2002), Evangelou et al. (2007), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Evangelou et al. (2007) Ghosh and Singh (2005) Andrej et al. (2005), Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000) Greger (1999), Griga et al. (2002), Landberg and Greger (1996), Rulford et al. (2002), Robinson et al. (1998), and Yankov et al. (2000) Evangelou et al. (2007) Baker and Walker (1990), Brown et al. (1995), Ernst (1968), Escarre et al. (2000), Greger (1999), and Robinson et al. (1998) Griga et al. (2002), Vassilev and Zaprianova (1999), and Yankov et al. (2000)

Ipomoea carnea Linum usitatissimum

Medicago sativa Mentha piperita

Nicotiana tabacum

Phacelia boratus Phragmites karka Populus sp.

Salix sp.

Sinapis alba Thlaspi caerulescens

Zea mays

(Ambrosia artemisiifolia), hemp dogbane (Apocynum cannabinum), Asian dayflower (Commelina communis), and nodding thistle (Carduus nutans) (Berti and Cunningham, 1993). Krishnasamy et al. (2004) identified Pb′s strongest accumulator to be Fioria vitifolia (Purakayastha and Chhonkar, 2010). Zinc: T. caerulescens has been established as a large Zn and Cd accumulator in initial phytoremediation research experiments, but its slow small size and growth rate are the major phytoremediation limitations of this plant (Black, 1995; Brown et al., 1994, 1995; Escarre et al., 2000). Current research demonstrates that moderately accumulating

398  Chapter 16 high-biomass plants such as Indian mustard (B. juncea) will generate four times as much Zn as T. caerulescens because it produces 10 times more biomass than this (Table 16.1) (Ebbs et al., 1997; Nanda Kumar et al., 1995; Purakayastha and Chhonkar, 2010; Salt et al., 1995). Cadmium: T. caerulescens has been documented regarding the ability to hyperaccumulate Cd (and Zn) for an extended period (Ernst, 1968). Several fast-growing trees (Salix, Populus) and high biomass crops such as tobacco (Nicotiana tabacum), oilseed rape (B. napus), peppermint (Mentha piperita), flax (Linum usitatissimum), cotton (Gossypium hirsutum), triticale, and maize (Z. mays), cereals, Indian mustard (B. juncea), and sunflower (H. annuus) are also optimal phytoextractors being able to compensate the lower levels of Cd accumulation with significantly higher yields of biomass (Bauddh and Singh, 2015; Bauddh et al., 2016; Griga et al., 2002; Purakayastha and Chhonkar, 2010; Yankov et al., 2000). Other research conducted by Ebbs and Kochain (1997) reported that Indian mustard (B. juncea) shows more tolerance to Cd than rape (B. rapa) and B. napus. Ghosh and Singh (2005), stated that Ipomoea carnea is more efficient than B. juncea in extracting Cd from the soil. I. carnea preceded by Phragmites karka and Datura inoxia are the most appropriate plants for Cd phytoextraction once the entire plant or aboveground biomass has been harvested (Table 16.1) (Purakayastha and Chhonkar, 2010). Arsenic: Brake fern (Pteris vittata L.) successfully accumulates As (up to 2.3% in its leaves) and generates a great quantity of biomass (until up to 1.7 m in height), making it feasible to be used for soil remediation applications (Ma et al., 2001). It has been found that Chinese brake fern is highly efficient for arsenic translocation to its fronds (Tu et al., 2002). Ampiah-Bonney et al. (2007) indicated that the Leersia oryzoides (rice-cut grass) has As uptake similar to the duckweed (Lemna gibba L.) and coincided with the value range mentioned for Chinese brake fern (P. vittata L.) (Table 16.1) (Purakayastha and Chhonkar, 2010). Mercury: Hg is not available for uptake in most polluted soil and mine tailings. Hg accumulation in the Berkheya coddii nickel hyperaccumulator, the salt-tolerant Atriplex canescens, and the Lupinus sp. and B. juncea nonaccumulators was tested in pot trials containing treated mine tailings with soluble Hg and sulfur-containing ligands. The results show that there is probable induced Hg accumulation of plant and for the remediation of Hg contaminated locations. However, issues about Hg volatilization and leaching need to be addressed before this phytoremediation method can be applied in the field (Moreno et al., 2004).

16.6.3  Advantages and limitations of phytoremediation Phytoremediation may be successfully used for the decontamination of macronutrients such as phosphate and nitrate (Horne, 2000; Sundaralingam and Gnanavelrajah, 2014), trace and nonessential elements such as Pb, Cu, Zn, Cd, Fe, As, Mn, Ni, Mo, Cr, Co, F, Hg, Se, V, and W (Blaylock and Huang, 2000; Cherian et al., 2012; Horne, 2000; Lytle et al., 1998), 238U,

Gold mining industry influence on the environment  399 137

Cs, and 90Sr radioactive isotopes (Dushenkov, 2003; Yadav and Kumar, 2019), organic solvents (Shang and Gordon, 2002), herbicides, and petroleum hydrocarbons (Olson et al., 2007; Schnoor et al., 1995). Phytoremediation includes several technologies for detoxifying the environment and has a variety of advantages and disadvantages. Phytoremediation possesses some particularly significant advantages (Aisien et al., 2012; Doty and James, 2007; Laghlimi et al., 2015): cost-effective because of the energy-consuming equipment absence and limited maintenance; environmentally friendly; suitable for a wide variety of toxic metals; simultaneous remediation of multiple or combined contaminants; improved esthetics; in situ, self-regulating system; soil erosion control surface water drainage prevention, reduction of infiltration and fugitive dust emissions, and favorable public perception. On the other hand, it also suffers some serious limitations. Phytoremediation is often a slow and incomplete process, which may take many years to remediate a site and is only applicable to surface soils (Laghlimi et al., 2015). Due to the chosen plants’ shallow root penetration, this method is confined to areas with shallow contamination, within the roots zone of remediating plants. It is constrained to sites with low concentrations of pollutants and has reduced capacity to transfer contaminant mass to the treatment area or root zone. Because contaminants are bioaccumulated in the vegetation, harvested plant biomass after the process of phytoextraction can be considered as hazardous waste; therefore, attention should be paid to disposal. Climate conditions are a limiting factor, depending on the local climate and growing season. The introduction of exotic species can disturb biodiversity and plants are susceptible to infestation and disease (Aisien et al., 2012; Doty, 2008; Ghosh and Singh, 2005; Hasanuzzaman and Fujita, 2013; van Aken et al., 2013).

16.7 Conclusions Phytoremediation is a “green clean,” plant-based remediation system, an efficient and cost-effective decontaminating technology for a diversity of organic and inorganic toxic contaminants. Inorganic contaminants occur as natural components of the earth’s crust and anthropic activities, including mining and industry, facilitate their release into the environment, contributing to soil and water contamination. They cannot be degraded, but they can be phytoremediated through plant root system stabilization or accumulation in plant shoot system. Phytoremediation can be widely used for the treatment of various solid, liquid, and gaseous substrates, in the decontamination of macronutrients (phosphate and nitrate), various elements (Pb, Cu, Zn, Cd, Fe, As, Mn, Ni, Mo, Hg, etc.), radioactive isotopes (238U, 137Cs, and 90Sr), petroleum hydrocarbons, organic solvents, and herbicides.

400  Chapter 16 The gold mining industry is a continuous pollution trigger, representing the primary source of heavy metal contamination during the exploitation and for many decades after the mining activity is ceased if the mining area is not environmentally cleaned. Phytoremediation technology can, therefore, represent a low-cost option for the remediation of industrially contaminated areas, especially for abandoned mines.

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CHAPTE R 17

Potential of Purun tikus (Eleocharis dulcis (Burm. F.) Trin. ex Hensch) to restore the Iron (Fe) contaminated acid mine drainage by using constructed wetland Nopi Stiyati Prihatinia and Soemarnob a

Department of Environmental Engineering, Lambung Mangkurat University, Banjarbaru, Indonesia Department of Soil Sciences, University Brawijaya, Malang, Indonesia

b

17.1 Introduction Coal mining activities in developing countries, including Indonesia, are still using open-pit methods. Mining in the open pit does not require complex technology and lower investment costs compared with underground mining. It is also associated with the existence of the coal which is generally in near the earth surface. Mining with open-pit is done by removing the surface soil and soil organic matter. The result is a layer of rock containing sulfur will react with water or oxygen, and thus releasing sulfate into the environment. This reaction causes acidity in the soil and water. This phenomenon is also known as acid mine drainage (AMD). AMD contains sulfuric acid and iron (Fe) compounds, which can flow out of the mining area. Water containing these compounds is acidic. When the acidic water is passed through the rocks/lime will dissolve compounds Ca and Mg of the rock. Waste acidic mining could cause corrosion and dissolve metals that contaminated water is toxic and can destroy aquatic life in a water body. Several methods have been applied to reduce the negative impact of acidic mining wastewater. A common method used (the conventional method) is to add certain chemicals (such as alum, Poly Aluminum Chloride/PAC, and Nalcolyte) on acid mine water before discharging into the environment (water body). Because it involves the use of chemicals and needs a huge cost to process the wastewater. Therefore, a wastewater treatment system that is cheaper than developed. One of the technologies being developed in recent years in some countries is a wastewater treatment system with a constructed wetland (CW).

Phytorestoration of Abandoned Mining and Oil Drilling Sites. https://doi.org/10.1016/B978-0-12-821200-4.00015-7 © 2021 Elsevier Inc. All rights reserved.

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410  Chapter 17 The CW system is engineered deliberately designed and created by leveraging a natural process in which the vegetation of wetlands, soil, and the microbial group associated in the wetlands help the process of wastewater treatment. CW designed to take advantage as much as the process that occurs in natural wetlands, but of course with controlled several environmental parameters. Some of the wetland has been designed and operated with only one purpose only, namely wastewater treatment, while the other wetland implemented for more than one purpose, such as using the outflow of wastewater for the restoration of wetland habitats for wildlife and improvement of environmental quality (USEPA, 1993). The wetland has been used internationally with good results. In 2000 alone there were 600 projects CW in the United States (USEPA, 2000) and more than 400 projects in Europe. CW in Indonesia has been used to improve the water quality of the River Basin (Meutia et al., 2003). A study had been carried out in Indonesia, precisely in the center of Surabaya Urban Development Community in 2007 to look at the ability of Sub Surface CW horizontal flow to treat domestic wastewater. This study shows that CW has lower capital and operating costs than conventional wastewater treatment with equivalent performance, so it becomes an attractive alternative for treating wastewater (Soewondo and Akbar, 2007). These studies also show that the CW can be implemented both in Indonesia and very potential to be applied in the treatment of other types of waste, including mining wastewater. CW using certain plants that is tolerant and can absorb contaminants, usually macrophytes. The plant is part of the components that affect the performance of the CW system. However, the mechanism of the role of plants in this system cannot be described because of differences in metabolism in each plant species. The use of local species or native species is more recommended applied to the selection of plants to be used in CW (Hoffmann et al., 2011). Purun tikus is the natural vegetation in the swamp area that lived inland with the characteristics of acid sulfate soils and so potential to be used in a CW. Data from Department of Industry, Trade, and Investment (Industry and Trade and the Prime Minister) Barito Kuala in Rahadi (2007) stated that in 2006 the species distribution of Purun plant would in the Barito Kuala have reached ±  713 ha, including Lepironia ±  641 ha and Purun tikus ±  72 ha (Rahadi, 2007). Previous studies have shown that Purun tikus can also serve to reduce the amount of dissolved Fe content in the boxes planted with rice and water from the waste coal mine, producing Fe absorption average of 1.1766 mg L−  1 and total dissolved solids (Sabokrouhiyeh et al., 2016) by an average of 0.4505 mg L−  1, in addition to the Purun tikus itself including an aquatic plant that has habitat with spectrum (distribution and abundance) are very broad, and relatively fast growth (Krisdianto et al., 2006). Ability Purun tikus that can live in wetlands and also that can absorb acids and certain metals contained in the coal mine wastewater is very interesting to observe. Therefore, this paper will present various information relating

Potential of Purun tikus to restore Iron contaminated acid mine  411 to the Potential of Purun tikus (E. dulcis (Burm. F.) Trin. ex Hensch) to restore the Iron (Fe) contaminated AMD by using the CW.

17.2  Geography and ecology on Purun tikus (E. dulcis) Purun tikus (E. dulcis) (Fig. 17.1) is one of the plants that are found in South Kalimantan. Purun tikus classification according to Steenis (2003) as follows: Division: Spermatophyta; Subdivision: Angiosperms Class: Monocotyledoneae; Order: Cyperales; Family: Cyperaceae; Genus: Eleocharis; Species: Eleocharis dulcis (Burm. f.) trinius ex Henschel (Steenis, 2003). Purun tikus is a weed that grows and develops in tidal swamp muddy. This plant belongs to the family Cyperaceae. Purun tikus stem is cylindrical and has a diameter of 2–3 mm, height can reach 150 cm, unbranched, leafless green, and so photosynthesis performed by the stem. Flowers are on the tip of the rod (Indrayati, 2011). Purun tikus has rhizome roots, during the first 6–8 weeks the rhizomes will form a seedling. The flower appears after seedling growth on the surface of the water which is more than 15 cm. After flowering the plant will form new roots at the end of the root with the length of 12.5 cm. After the age of 7–8 months rhizome becomes unproductive and then stems begin to dry up and will slowly die (Indrayati, 2011). This plant is a perennial herbaceous plant that is upright, with the elongated stolon (Fig. 17.1) colored brownish to black. Purun tikus have roots, stems, tubular green leaves, and flower. Purun tikus stem is upright unbranched, grayish-green to shiny with a length of 50–200 cm with a thickness of 2–8 mm. Leaves Purun tikus narrowed down to the basal stems, such as membrane, the end is not symmetrical, reddish-brown to violet. Flower Purun tikus are usually produced by plants that grow vegetatively, located in the terminal part of the rod

(A)

(B)

Fig. 17.1 Purun tikus (Eleocharis dulcis (Burm. f.) trinius ex Henschel); (A) Old Purun tikus were connected by a stolon, (B) Purun tikus in Village Puntik, South Kalimantan.

412  Chapter 17 with a length of 2–6 cm and a width of 3–6 mm and are hermaphrodites (Steenis, 2003). At an altitude of up to 1350 m above sea level, Purun tikus will germinate at the soil with temperatures above 14°C.

17.2.1  Habitat Purun tikus Purun tikus can be found in open areas flooded by saltwater, brackish water, and freshwater at an altitude of 0–1350 m above sea level. The plant is also commonly found in rice fields and stagnant water. Purun tikus can grow well at a temperature of 30–35°C and soil moisture of 98%–100%. Land that is preferred for its growth is the type of soil or humus to pH 6.9–7.3, but also be able to grow well in the soil slightly acid (Flach and Rumawas, 1996). These plants are specific for acidic sulfate soil because of its resistant to high soil acidity (pH 2.5–3.5), and then become the vegetation indicator for acid sulfate soils (Noor, 2004). Purun tikus also can grow on the soil with extreme chemical properties, such as low pH and high soluble Al content, high SO 4 2− (content can be changed by other compounds), and high soluble Fe. Purun tikus can grow at pH 3, the content of aluminum (Al) of 5.35 mEq 100 g−  1, the content of soluble sulfate ( SO 4 2− ) 0.90 mEq 100 g−  1, and the content of soluble iron (Fe2  +) at 1017 ppm (Priatmadi et al., 2006). These plants can also be propagated by seed or corm. For planting, the corm is placed in a shaded place for 2–3 days and then soaked in water for 2 days. After that, the corm is planted in beds covered, with spacing in the form of a rectangle measuring 50–100 cm or triangle measuring 45–60 cm × 45 cm. After planting, the soil is flooded for 24 h and then left it (Wardiono, 2007).

17.2.2  Utilization Purun tikus These plants have many benefits. Corm can be used for raw or cooked vegetables to a wide range of cuisines such as gravy, salads, omelets, with dishes of meat or fish, even as food or cake. The big corm is great eaten fresh as a substitute for fresh fruit, the smaller corm can be made to flour and chips. The leaves can be used for cattle feed, mulch or compost, sleeping mats, and clothes. The juice of the corm contains antibiotics “puchiin” that effective against Staphylococcus aureus, Escherichia coli, and Aerobacter aerogenes (Wardiono, 2007). It’s just that in the area of Kalimantan Purun tikus corm are very rarely found. Purun tikus are used more as craft materials, as raw material for bioboard (Rahmawati et al., 2019), Purun tikus fibers begin to be used for reinforcement in composites as a substitute synthetic fiber (Syarief, 2011). According to Suriadikarta and Abdurachman (2000), Purun tikus was used in overcoming problems in acid sulfate soil reclamation. Purun tikus is capable of absorbing N of 1.45%;

Potential of Purun tikus to restore Iron contaminated acid mine  413 P 0.08%; K 2.05%; Ca 0.22%; Mg 0.16%; S 0.18%; 1386 ppm Fe; Mn 923 ppm; Cu 15 ppm; Zn and 48 ppm. From that research, it turns out purun tikus is very helpful in keeping the land degradation, particularly potential acid sulfate soil (Suriadikarta and Abdurachman, 2000). A study carried out to know the ability of the Purun tikus absorb Pb in wastewater palm, Pb concentration in the plant was measured at the roots and stems. The concentration of Pb in the roots was higher than in the stem of the plant (Prihatini et al., 2011). This is because the roots directly in contact with wastewater and sediment that are on the bottom, as well as their efforts to localize the material toxic into the body so that the poisoning can be prevented and the process of metabolism is inhibited so that the metal is bound by chelating molecules. Accumulation of Pb into the plants through the process of passive absorption or uptake process. The process of uptake of back and forth and going in quick time. This process occurs on the surface of cells, living cells, as well as the dead cell from biomass. The process of uptake will last more effective if they are supported by the pH and other ions in the media in which heavy metals can be deposited as a salt that does not dissolve (Onrizal, 2005).

17.2.3  Nutrients need The plant including Purun tikus needs some kind of nutrients during its growth and development. Nutrients that are important for plants can be divided into macronutrients and micronutrients based on the required amount that plants need. The macronutrients required by plants are 0.1% (1000 ppm) or more, and micro-nutrients in concentrations of less than 0.1%. The elements that belong to macronutrients such as N, P, K, Ca, Mg, and S, while belonging to micro-nutrients, such as Fe, Mn, B, Mo, Cu, Zn, and Cl (Lakitan, 2008). Each nutrient has a different function and affects certain processes in the development and growth of plants. Nitrogen is a major component of various compounds in the body of plants, i.e., amino acids, proteins, chlorophyll, and alkaloid. Approximately 40%–45% of protoplasm is composed of a compound containing N (Agustina, 2004). Nitrogen is required for the formation of the vegetative part of the plant, such as leaves, stems and roots, besides playing a role in the formation of chlorophyll which is useful in the process of photosynthesis, forming protein, fat, and a variety of organic compounds (Foth, 1998). Phosphorus plays an important role in energy transfer in plant cells, such as ADP and ATP (Agustina, 2004). Phosphorus stimulates root growth, especially the roots of young plants, accelerates the growth of young plants into mature plants, helps assimilation and respiration, and as a raw material for the formation of certain proteins. Potassium works in the setting mechanism such as photosynthesis, translocation of carbohydrates and protein synthesis, strengthens the body plant, improves plant resistance to drought, and plays a role in the mechanism of the process of photosynthesis (Foth, 1998).

414  Chapter 17 Most of the nutrients absorbed by plants from the soil through the roots, but carbon and oxygen from the air are absorbed by the leaves. The root system is controlled by a genetic trait of the plant but can also be influenced by the condition of the ground. Factors affecting the spread of the roots, i.e., soil temperature, aeration, water availability, and the availability of nutrients. Grass species have a fibrous root system that spreads superficially near the soil surface (Lakitan, 2008). The root moves to the area where the soil solution contains nutrients that can be transported to the root surface. Nutrients transported from the soil solution to the root surface occurs in two ways, namely, mass flow and diffusion. The mechanism of mass flow is a mechanism of movement of nutrients in the soil toward the root surface together with the mass movement of water. During the process of transpiration takes place, plant roots absorb water. The movement of water mass to the root carries the nutrients contained in the water (Agustina, 2004). The availability of nutrients to the root surface can also occur through a mechanism of different concentrations. In the root surface, the concentration of nutrients is lower than the soil solution. This condition occurs because some of the nutrients have been absorbed by the roots. The high concentration of nutrients that cause the occurrence of diffusion of highly concentrated nutrients to the position of the root surface (Foth, 1998). The process of mass flow and diffusion occurs by different physical properties and different directions of motion. The mass flow of a substance in a soil solution will move from an aqueous area to a dry area. While diffusion is just the opposite, that is, from areas of high concentration to low concentrations (areas with a lot of water). Although the process is different, in the soil it takes place simultaneously or together (Wild, 1981). Both process, diffusion and mass flow, are very important in moving nutrients from somewhere to the surface of the root so that they can be absorbed by the plant roots. This is the case for P, K, Ca, Mg, S, and so on, but for N elements, especially NO−  3, the movement does not only move near the root but in transport away from the root or is commonly known as purified/leached (Nkrumah et al., 1989).

17.3  CWs planted with Purun tikus CW planted with Purun tikus (E. dulcis) has been shown to have a high efficiency of removal of Fe in AMD (Prihatini, 2016; Prihatini et al., 2015, 2016b, 2017a,b; Prihatini and Soemarno, 2017; Yunus and Prihatini, 2018). CW performance can be seen from its ability to reduce levels of pollutants or parameters (Suswati and Wibisono, 2013). Most of the models seen in the efficiency rate expressed in percent (%). However, the efficiency cannot explain how much iron or other pollutants per unit of time is removed or unit surface area of wetland. Therefore, in several other studies, the performance of the CW model can be seen from the amount of iron removed per unit time (days) (Hedin and Nairn, 1990).

Potential of Purun tikus to restore Iron contaminated acid mine  415 The CW technology is widely used to treat acid mine drainage (Hedin, 2008; Hedin and Nairn, 1990; Johnson and Hallberg, 2005; Kleinmann, 1990; Lesley et al., 2008; Sheoran and Sheoran, 2006; Vesper and Smilley, 2010; Younger et al., 2002; Zhang et al., 2010). The CW is a complex system with many components that work together, so that differences in these components affect the performance of the CW. The main component that determines CW performance is aquatic plant species that are suited to the characteristics of wastewater (Supradata, 2005). The most important operational factor of CW are the flow of wastewater, hydraulic loads, and detention time (Faulwetter et al., 2009). Based on the wastewater flows, it can be divided into the batch flow and continuous flow. In the batch flow system, the CW is supplied with wastewater over some time and after that no additional wastewater (Tchobanoglos et al., 2003). In the continuous flow system, the wastewater flows continuously into the CW (Tchobanoglos et al., 2003; Faulwetter et al., 2009). A study was conducted to determine the performance of the horizontal subsurface constructed wetland (HSSF-CW) with Purun tikus aquatic plant in removing soluble Fe, and raising the pH of AMD, involving the flow batch system and the continuous flow system. The result of the study shows that the HSSF-CW with the Purun tikus plant capable of removing iron and raising the pH of the AMD and the HSSF-CW model with a continuous wastewater flow has better performance as compared to the HSSF-CW model with the batch flow (Prihatini, 2015). Batch system can increase the capacity of elimination of pollutants (Schultz Jr, 2007; Stein et al., 2003, #65), especially for CW to treat domestic waste (Caselles-Osorio and Garcia, 2007). However, research on Burgoon et al. batch system is not better than the continuous system (Burgoon et al., 1995). As a result of Prihatini and Soemarno (2017) and Prihatini (2015) study, the HSSFCW batch system appears to perform no better than the HSSFCW continuous system (Prihatini et al., 2015). This is due to the removal of heavy metals such as iron from the solution in the wetlands is controlled by the interaction of the plant uptake, microbial activity, biodegradation, phytoaccumulation, photodegradation, cation exchange, co-precipitation, sorption, deposition process, and sedimentation (Sheoran and Sheoran, 2006). The pores of the media are saturated by water resulting in no more room for oxygen. While oxygen is necessary for the oxidation of iron that can be a compound that can precipitate (precipitated). In contrast to the continuous system of wastewater is not put into the reactor, as well as a batch system, thus providing an opportunity for the oxidation process to take place better. Besides, the matrix soil as a medium in SSFCW has a decisive influence on the process of hydraulic and affect system performance. The land is the main material support for the growth of plants and microbes. This is one aspect of the complex processes that occur in the rhizosphere interactions between roots/rhizomes and soil matrix (Stottmeister et al., 2003). Another study published event was conducted limited compared to performance wetland subsurface flow with horizontal subsurface flow constructed wetlands (HSSFCW) and

416  Chapter 17 vertical flow subsurface constructed wetlands (VSSFCW). VSSFCW can set aside iron more with less time and can increase the pH greater than HSSFCW (Prihatini et al., 2015). This is consistent with research that has been done and is intended Risnawati and Damanhuri (2010) which concluded that the removal of Fe, Cu, and Zn in the leachate using CW with Cyperus papyrus reaches more than 90%. Elimination of iron in a horizontal reactor is 91.38% and the vertical reactor 95.44%. Cu in the reactor 98.15% horizontal and vertical reactors 97.28%, and the allowance for Zn in the horizontal reactor at 97.71% while 97.54% of the vertical reactor (Risnawati and Damanhuri, 2010). In Prihatini and Soemarno (2017) and Prihatini (2015) research, vertical flow used a vertical downward flow. In vertical downward flow type, water flowed into the wetland from the top layer of media channels and outlets made in the bottom of the media, so that water will flow down through the root zone by gravity. Systems such as this allow the flow of acid mine water flows evenly in CW thus increasing the chance of contact with the root zone of plants. In vertical flow CW only required uniformity distribution root on the top layer (the first 10 cm), while the HSSFCW-uniformity distribution of rooting around in the media is very important (Hoffmann et al., 2011). In HSSFCW acid mine water flowing horizontally through the center of the media CW, the water will flow through the root zone and then out through the outflow channel. Performance is highly dependent on the contact time between the AMD with the media and the root zone, and the concentration of iron in AMD.

17.4  Role of Purun tikus in constructed wetland Role of Purun tikus (E. dulcis) in Constructed Wetland shown by research Prihatini et al. (2015). The study used CW is the CW-type of Horizontal Subsurface Flow (HSSF) with two kinds of wastewater flowing ways, batch-flow (model A) and continuous-flow (model B). The media used are acid sulfate soils from the Central Puntik Village, South Kalimantan, which is a natural habitat for Purun tikus. The thickness of soil for plant growth medium in each reactor is 30 cm. In this study, the HSSF-CW is planted with Purun tikus. Seedlings planted are tillers with an average height of 15 cm, the seedlings were planted at a distance of 10 cm. Results showed differences between the HSSF-CW without Purun tikus (HSSF-CW control) and the HSSF-CW planted with Purun tikus (model A and model B) (Fig. 17.2). This suggests that Purun tikus aquatic plants played a significant role in the process of removal of dissolved Fe from AMD. Purun tikus supplied oxygen (O2) necessary in oxidizing and precipitating iron substances, and Purun tikus is also able to absorb the amount of Fe for their metabolism (Stottmeister et al., 2003). Both of these processes are estimated to be the cause of lower concentrations of dissolved Fe in the effluent of the HSSF-CW with Purun tikus compared to the HSSF-CW without plants. Most of the elements that plants need to be absorbed from the soil solution through the roots, but carbon (C) and oxygen (O) are absorbed through the air by the leaves. Absorption

Potential of Purun tikus to restore Iron contaminated acid mine  417

Fig. 17.2 The concentration of Fe AMD effluents in the HSSF-CW control (without vegetation), Model-A (vegetated with a batch of flow), Model-B (vegetated with the continuous flow).

of nutrients is generally slower than the water absorption by plant roots. Plant root systems are more controlled by the genetic characteristics of the plants concerned, but it has also been proven that the plant root systems can be influenced by soil conditions or plant growth media. Factors affecting the pattern of spread of plant roots include mechanical barriers, soil temperature, aeration, water availability, and nutrient availability. Nutrient uptake is accumulative, selective, one-way (unidirectional), and cannot be saturated (Lakitan, 2008). Water and nutrients are absorbed by the plant roots, the absorption of nutrients is divided into three ways: the diffusion, mass flow, and root interception. Water and nutrients are dissolved in it, called the soil solution, move through the soil to reach the roots of plants. Furthermore, from this process, the absorption of water and nutrients by plant cells occurs with a different mechanism. Mechanism of nutrient fulfillment by plants in three ways, namely: (1) Mass flow is the absorption of organic matter through the movement of nutrients present in the soil in a moving water mass. (2) Root interception occurs when the roots of plants grow into the space occupied by nutrients and there is very close contact so that ion exchange occurs on the surface of the roots and the surface of the adsorption complex. (3) Diffusion is the absorption of nutrients by the root of the soil solution, other dissolved nutrients move toward the root without mass flow, the principle of diffusion is the movement of the concentrated area of each high element toward the area that concentrates each lower element (Rivando, 2011). Plants can absorb ions from the environment into the body through the cell membrane. Two properties of ion absorption by the plant is: (1) Concentration factor; the ability of plants to accumulate ions to a certain concentration level, even to achieve some level greater than the concentration of ions in the medium,

418  Chapter 17 (2) Differences in quantitative nutrient requirements of different types on each plant. The cells of the roots of plants generally contain a concentration higher than in medium vicinity. A large number of experiments show that there is a relationship between the rate of consumption of the ion concentration that resembles the relationship between the reaction rate delivered enzyme with substrate concentration. This analogy shows that there is a special barrier in the cell membrane that is only suitable for a particular ion and can absorb ions so that the substrate concentration is high all the barriers play a role in the maximum rate until it reaches the rate of consumption of saturated (Fitter and Hay, 1991). Aquatic plants/wetlands play an important role in the biogeochemical cycle of trace elements through the active and passive cycles of these elements. They act as “pomp” for essential and nonessential elements. Absorption of elements by plant tissues causes immobilization of elements in plant tissues and wetlands so this is very significant for wastewater treatment (Prasad et al., 2006). Based on mobilization in the rhizosphere which is controlled by the chemical reaction of the soil, the metal will be absorbed by the root cells. Absorption of these metals across the plasma membrane is mediated by protein transport and intracellular binding sections with high affinity. Several studies have shown that hyperaccumulation of Zn and Cd by Thlaspi caerulescens involves an increase in absorption/uptake of metals by the roots. Several Zn transporter genes have recently been cloned from T. caerulescens, these genes belong to the ZIP family (Zn-regulated transporter/Fe-regulated transporter-like proteins). These genes are called ZNTl and ZNT2 which have been proven to be present in the roots of T. caerulescens, but the presence of these genes is not responsive to the status of Zn in plants. Through functional complementation in yeast, it shows that ZNTI mediates the absorption of high affinity from Zn2  + and absorption of low affinity from Cd2  +. Specific changes in Zn-responsive elements, such as transcription activators, might play an important role in the hyperaccumulation of Zn in T. caerulescens. However, the increased absorption of Cd by T. caerulescens cannot be explained by the Zn transport pathway but may be related to increased expression of the IRT1 gene, which is important for Fe absorption. IRT1 gene is proven to be able to mediate the absorption of high-affinity Cd2  + in Arabidopsis thaliana plants. Several protein classes have been involved in transportation in plants, including the metal P-type ATPase involved in overall ion homeostasis and tolerance regulation in plants, protein-related natural resistance macrophage proteins (NRAMP), and diffusion cation facilitators of protein groups. ATPase type CPx has been identified as being present in various organisms and has been involved in the transportation of hazardous metals such as Cu, Cd, and Pb throughout the cell membrane. This transporter uses ATP to pump various substrates across the cell membrane. P-type Arabidopsis ATPase is the first CPx ATPase reported in plants. The type of CPx ATPase identified so far has been involved in Cu transportation. The physiological role of metal transporters in higher plants is not clearly known.

Potential of Purun tikus to restore Iron contaminated acid mine  419 Because Arabidopsis CPx ATPase transports different substrates that may be present in the membrane and functions as efflux pumps, it can also be present on intracellular membranes responsible for metal compartmentalization, for example, absorption in vacuoles, Golgi, or endoplasmic reticulum. Because cellular concentrations of metals must be carefully controlled, transporters are good candidates for this arrangement (Prasad et al., 2006). Soil is the main source of metal for plants, so that efficient absorption is needed for the survival of the plant life. Although the metals in the soil are in large quantities but cannot be accessed because plants can only absorb metals in dissolved form. Monocot plants generally use a method based on the formation of chelate (chelation-based strategy) to overcome some metals that are not obtainable (Palmer and Guerinot, 2009). Chelate is a complex compound produced by organic ligands that bind metal ions with more than one functional donor group. These bonds form heterocyclic rings called chelate rings (Tan, 2010). It is not yet known about the mechanism of absorption of Fe by Purun tikus, but as a species, in the monocot Purun tikus class, it might use chelation-based strategy to absorb Fe. This strategy uses the release of chelators called phytosiderophores into the rhizosphere to bind Fe+  3 and bring it into the plant. Phytosiderophores are synthesized from methionine and usually refer to the mugineic acid family (Mas) (Lambers et al., 2008; Palmer and Guerinot, 2009). The intracellular metal journey in monocotyledonous plants including Purun tikus begins with the absorption of Fe along with Zn, which is absorbed as phytosiderophore chelates (Lambers et al., 2008; Palmer and Guerinot, 2009) by YSL transporters in the epidermis. Fe can also be absorbed by OsIRT1. The metals move through the symplastic space to the vasculature by passing through the soft Casparian gap in the endodermis. Citrate effluxer FRDL1 is very important to transport Fe to shoots through transpiration. Fe is transported from phloem by OsYSL2 and OsIRT1 to shoots and seed tissue. MA is mugineic acid and NA is nicotianamine (Palmer and Guerinot, 2009). Purun tikus meets the requirements as a plant suitable for phytoremediation, including having fast growth capabilities, producing large biomass, tolerant, and being able to accumulate metals (Prihatini and Soemarno, 2017) and storing them in plant bodies in high concentrations, easily cultivated, and harvested (Karenlampi et al., 2000). Phytoremediation is defined as the sweeping of pollutants mediated by plants. Sweeping can mean the destruction, inactivation, or immobilization of pollutants into harmless forms (Chaney et al., 1995). There are five ways in which plants play their role in the process of phytoremediation of metalpolluted soils, namely rhizofiltration, phytoextraction, phytotransformation, phytostimulation, and phytostabilization. Rhizofiltration is the process of plants absorbing metals and being held at the root and prevented from going to the upper biomass. This mechanism, in addition, can prevent metal-poisoning plants while at the same time can avoid the movement of metals to a wider place and prevent the accumulation of metals into the food chain.

420  Chapter 17 Biochemical adaptations involve molecular changes, the speed and pattern of reaction chains or the metabolic patterns of cells, tissues, and organs. This adaptation is greatly influenced by the time available for the organism to be able to respond to changes in the environment. Short-term responses can be seen in morphological and physiological changes. But if changes occur continuously until one or more plant development periods, there will be changes in acclimatization and naturalization (Haryanti, 2009). The availability of metal elements and their absorption by plants is determined by the total concentration and shape of the metal in the soil in addition to geochemical factors in the root zone. Genetic factors and plant species determine the absorption of metals in the root zone and root/canopy at varying rates. Absorption is also determined by the type of plant tissue and the treatment given to the soil (Knox et al., 2000). The metal will accumulate in plants after forming a complex with other elements or compounds, one of which is phytochelatin which is composed of several amino acids such as cysteine and glycine. Phytochelatin functions to form complexes with heavy metals in plants and functions as detoxification of plants from heavy metals if plants cannot synthesize phytochelatin causing growth retardation and leading to death. The highest levels of phytochelatin are found in plants that are tolerant of heavy metals (Hirata et al., 2001).

17.5  Purun tikus seedlings, planting space, and growth in the constructed wetland system Several factors including the age of the plant and seasonal variations can have an impact on the ability of plants to absorb contaminants. Optimization of these factors will help increase the role of plants in CW. In general, young roots grow faster and have a level of uptake is higher than older roots. Research carried out by Silva Gonzaga et al. Pteris vittata showed that 8 weeks of age and take translocate arsenic faster than plants aged 16 months, indicating that the young plants are most efficient for phytoextraction. However, Rofkar states that the age factor of Cordyline stricta and Spartina pectinata does not affect the absorption of arsenic by roots, but older plants receive arsenic transfer with a greater portion of leaves and stems than younger plants (Zhang et al., 2010). The study was carried on to determine the age and spacing Purun tikus most appropriate to maximize the functionality of biofilters Purun tikus in CW (Prihatini et al., 2016b), This is an attempt to optimize the role of the Purun tikus in CW. The study uses the horizontal subsurface flow CW (HSSFCW) using a continuous system. The measurement of the concentration of iron in samples of influent AMD is 25.44 ppm. The average Fe concentration in the effluent of the HSSFCW between 5.59 and 14.84 ppm. Decreased concentration of Fe occurs on all models the HSSFCW with Purun tikus in this experiment. The highest decrease in Fe concentration that is 78.05% occurred in the HSFCW model with purun tikus spacing of 15 cm and purun tikus tillers age (Fig. 17.3).

Fig. 17.3 The concentration of Fe in AMD and Efficiency of the HSSF-CW system planted with Purun tikus.

422  Chapter 17 Preliminary Fe due to the complex process that occurs at the HSSFCW includes the interaction of physicochemical and biological. These processes involve plants, mediums, and microorganisms that exist in (Munawar, 2007; Vymazal, 2010; Vymazal and Kropfelova, 2008; Younger et al., 2002). In general, the most significant of the plant in conjunction with the League of the water purification effect is brought about by the physical presence of the plant. Plants provide a large surface area for the attachment and growth of microbes (Hua, 2003), Complex interaction of plants with microorganisms is claimed as a key process to isolate the metal from the wastewater (Kosolapov et al., 2004). The pH and temperature also affect the interaction process. The influent pH of 3.00 while the effluent ranged from 4.80 to 5.55 pH in the HSSFCW is increased, the increase ranging from 1 to 2.55. The pH of HSSFCW effluent with purun tikus tiller 15 cm plant spacing was the biggest increase compared to other HSSFCW models (Prihatini et al., 2016b). The pH parameter is inversely proportional to the solubility of Fe and pH is directly proportional to the bacterial population. Increasing the pH caused a decrease in the solubility of Fe and trigger an increase in bacterial population (Fauziah, 2013). The pH value is low in acid mine drainage in large part because there is a lot of iron oxide sulfate (Williamson et al., 2006). Sulfate-reducing bacteria cause sulfate concentration decreases and causes an increase in pH. Reducing-sulfate oxidizes several organic compounds or hydrogen to reduce sulfate and sulfide form. Reduction of sulfate produces decreasing amounts of sulfates and increased bisulfide and HCO3  −. Gas hydrogen sulfide can be formed of bisulfide and hydrogen ions. The loss of H2S into the atmosphere and also the production of HCO3  − lower acidity and raise the pH (Kosolapov et al., 2004). Increasing the pH caused ferric ions (Fe3  +) oxidation and bind to the hydroxide Fe(OH)3, which is insoluble and precipitates and formed a reddish color on the substrate (Effendi, 2003). Model HSSFCW with Purun tikus tiller was the highest growth average (Prihatini, 2015). This suggests that Purun tikus can grow well with the spacing and age. Spacing is one way to keep the plant needs to be available equally to every individual and to optimize the use of available environmental factors. The distance between the individual plants that cause irregular growth will vary greatly, the plant will grow a little closer and the gap is growing larger following the availability of nutrients in the environment. The density of lead spacing narrow spacing between the clumps with other families. This led to greater competition in making environmental factors (Sitompul and Guritno, 1995), thus affecting the growth of purun tikus. Distance affects the availability of nutrients and the intensity of light needed by plants. It depends on the number of populations in the reactor If high-intensity light, then taking up CO2 and also improving the process of photosynthesis that affect plant growth. Age of plants to determine the number of different nutritional needs at every age level. Supplies nutrients decline with increasing age. Purun tikus, as well as most other plants,

Potential of Purun tikus to restore Iron contaminated acid mine  423 require Fe as one constituent of chlorophyll, proteins, enzymes, and plays a role in the development of chloroplasts. The roots of new and more active root hairs in absorbing iron. The mechanism of Fe absorption by Purun tikus is not known yet. Purun tikus may use a chelation-based strategy to absorb Fe like other monocotyledonous plants. This strategy uses the release chelator called phytosiderophores into the rhizosphere to bind Fe+  3 and bring it into the plant. Phytosiderophores synthesized from methionine and usually refers to Mas (Lambers et al., 2008; Palmer and Guerinot, 2009). Together with Zn, Fe absorbed as phytosiderophore chelates (Lambers et al., 2008; Palmer and Guerinot, 2009) by YSL transporters in the epidermis. Fe can also be absorbed by OsIRT1. The metals are moving through chamber symplastic toward the vasculature through a Casparian pathway in the endoderm. Citrate effluxer FRDL1 (a protein transporter) is very important to transport Fe to shoot through transpiration. Fe transported from the phloem by OsYSL2 and OsIRT1 to the sprout and seeds tissue (Briat, 2007; Briat and Lobréaux, 1997; Jeong and Connolly, 2009; Kim and Guerinot, 2007; Palmer and Guerinot, 2009; Samiotakis and Ebbs, 2004; Solti et al., 2012; Yoshida and Negishi, 2013). Plants accumulate metals by forming metal complexes with other elements or compounds, one of which is phytochelatin which is composed of several amino acids such as cysteine and glycine. Phytochelatin functions to form a complex with heavy metals in plant sand serves as detoxification of heavy metals from the plant, if the plant cannot synthesize phytochelatin can cause growth retardation and lead to death. Plants that tolerate to heavy metals have high rates of phytochelatin (Anjum et al., 2012; Cobbett, 2000; Hirata et al., 2001, 2005; Liu et al., 2006; Yadav, 2010; Yang et al., 2005).

17.6  Potential of purun tikus for iron accumulation in its tissues from acid mine drainage Iron as a micronutrient is only needed less than 0.1% or ±  1000 ppm for plant growth. In general, plants only need Fe as much as 50–250 mg kg‑1 of biomass in tissues. If the Fe content in the tissue exceeds 300 mg kg‑1 the plant is said to be poisoned. The high concentration of Fe in the Purun tikus organs (Fig. 17.4) makes this plant a potential hyperaccumulator plant for Fe (Prihatini, 2016) because it can absorb and localize these elements more than 0.1% in the body organs. Purun tikus contains many phenolic compounds in the root cell walls and stems which makes this plant have a high tolerance to Fe. The metal will accumulate in plants after forming a complex with phytochelatin. Phytochelatin detoxifies plants from heavy metals if plants fail to synthesize phytochelatin it leads to growth retardation and leading to death. The highest levels of phytochelatin are found in plants that are tolerant of heavy metals (Anjum et al., 2012; Cobbett, 2000; Hirata et al., 2001, 2005; Liu et al., 2006; Yadav, 2010; Yang et al., 2005).

424  Chapter 17

Fig. 17.4 Fe concentration in Purun tikus organs at VSSFCW system and HSSFCW system.

Fig. 17.5 Fe concentration in Purun tikus at VSSFCW system and HSSFCW system.

Model of the SSFCW with the Purun tikus plant capable of removing iron and raising the pH of the AMD (Prihatini et al., 2015). In that study, the concentration of Fe in the roots was higher than Fe in the stems at the VSSFCW, while at the HSSFCW Fe concentration in stems and roots in the first 10 days has increased, but Fe in stems decreased on the measurement of the 15th day whereas Fe in root increased. Results of statistical analysis using t-test showed that the average concentration of Fe in the roots is statistically different with an average concentration of Fe in the stems of Purun tikus at HSSFCW and VSSFCW (Fig. 17.5). Fe concentration in Purun tikus as a whole is shown in Fig. 17.5 which tends to follow the line of a polynomial equation as follows: VSSFCW : 2381.3 x 2  y  30207 x  139.75 with R 2  0.6233 HSSFCW : 1305.8 x 2  y  33736 x  1766.3 with R 2  0.9975 The model equation above can be used to predict the Purun tikus maximum accumulation time. Purun tikus had the highest Fe concentration on day 6 for VSSFCW and day 13 for HSSFCW. This shows that Purun tikus planted at VSSFCW reach maximum uptake for 6 days

Potential of Purun tikus to restore Iron contaminated acid mine  425 and 13 days at HSSFCW. After that period, we recommended the harvesting of Purun tikus and replaced it. However, further study is needed on the use of plants Purun tikus at CW applied in the field in the long term (Munawar, 2007). Plants wetlands including Purun tikus store nutrients and metals in biomass (Jacob and Otte, 2003; Schulz et al., 2003). The results Prihatini and Soemarno (2017) and Prihatini (2015), Fig. 17.6 shows that total Fe in plant Purun tikus are positively correlated with time (days). This shows that the amount of Fe in the Purun tikus will continue to grow along with the increase in time. On day three, Purun tikus have decreased total Fe for a minimum of research carried out (15 days). At the root (Fig. 17.7) and stem (Fig. 17.8) Purun tikus, total Fe also increases with time. The number represents how many Fe (ppm) in the Purun tikus planted area per reactor constructed wetland. If the amount of Fe continues to increase, the concentration of Fe in the Purun tikus will be even greater. Transporter proteins such as citrate effluxer FRDL1 very important in the process of transporting Fe to the area along with the shoots of plants transpiration stream. Fe can also be transported by the phloem tissue toward the tip and tissue of young plants (Briat, 2007; Jeong and Connolly, 2009; Kim and Guerinot, 2007; Palmer and Guerinot, 2009; Samiotakis and Ebbs, 2004; Solti et al., 2012; Yoshida and Negishi, 2013; Briat and Lobréaux, 1997). Risnawati and Damanhuri (2010) using the plant C. papyrus that has the same family with Purun tikus, family Cyperaceae, in HSSFCW for 9 days to remove the metal from landfill leachate. When compared results from Prihatini and Soemarno (2017) and Prihatini (2015) with the results of this research, E. dulcis (17,800.35 mg) accumulated Fe greater than C. papyrus (2553.01 mg) (Risnawati and Damanhuri, 2010). Another study that uses Purun tikus in VSSFCW with media variation shows that Purun tikus can uptake 4263 ppm Fe

Fig. 17.6 Relations total Fe Purun tikus with time (days).

426  Chapter 17

Fig. 17.7 Relations total Fe root Purun tikus with time (days).

Fig. 17.8 Relations total Fe stem Purun tikus with time (days).

within 5 days (Prihatini and Soemarno, 2017), this makes the Purun tikus high potential for use in phytoremediation. Phytoremediation uses plants that have the capability of rapid growth, produce large biomass, tolerant, and able to accumulate the metal and store it in the body of plants in high concentrations, and is easily cultivated and harvested (Karenlampi et al., 2000). In some studies using Purun tikus plants (Prihatini, 2015, 2016; Prihatini et al., 2016a; Prihatini and Soemarno, 2017; Yunus and Prihatini, 2018) based on previous studies have found that Purun tikus has a large spectrum of biomass habitat (distribution and abundance) are very broad,

Potential of Purun tikus to restore Iron contaminated acid mine  427 relatively fast growth and be able to accumulate metals (Hg and Pb) (Prihatini et al., 2011; Krisdianto et al., 2006). The ability of plants to absorb metals from the environment is shown by the bioconcentration factor (BCF), while the ability of metal translocation in plant organs shown by translocation factor (TF) (Prihatini et al., 2011; Rezvani and Zaefarian, 2011). BCF is a parameter to determine the potential of plants to accumulate metals, and this value is calculated in terms of the dry weight of plants (Tommy, 2009). The results from Prihatini and Soemarno (2017) and Prihatini (2015) showed that the Purun tikus would have the potential to accumulate iron (Fe) are shown with the BCF increased (Figs. 17.9 and 17.10). Plants with high BCF can be used as bioremediation agents. A high concentration of metals in the water is the main factor that affects the efficiency of the absorption of the metal. The accumulation of metals in plants allows further action to be carried out on metals contained in these plants. Utilization of plants with high levels of accumulation that will make it easier for further treatment so that levels of contamination can be reduced with minimal cost and volume of work. Fig. 17.11 (Prihatini, 2016), shows that TF (in concentration) showed a tendency to decrease. This suggests that the availability of iron for plants is very high, but its mobility in the plant body is very limited. A small TF value indicates that Purun tikus translates Fe from the root to the stem of Purun tikus in small amounts, more Fe is present in the root. So it can be said that purun tikus accumulates large amounts of Fe in the root and translocates Fe from the root to the stem in small amounts (Prihatini, 2015). Iron in the roots of Purun tikus can accumulate in the form of iron plaques. Iron plaque accumulation can explain the addition of root dry weight up to 10% and extend as much as 15–17 cm rhizosphere (Chen et al., 1980; Hansel et al., 2001; Taylor et al., 1984).

Fig. 17.9 The BCF and TF Fe VSSFCW batch system.

428  Chapter 17

Fig. 17.10 The BCF and TF Fe HSSFCW batch system.

Prihatini and Soemarno (2017) and Prihatini Research (2015) show that the relationship TF positively correlated with time (Fig. 17.11). This means if the biomass and the amount of Fe in the Purun tikus increased the value of TF bigger. Increased biomass showed that Purun tikus would experience good growth, while the increase of Fe showed the increasing number of Fe contained in the Purun tikus. The TF indicates a comparison/Fe ratio in the stem and root Purun tikus (Prihatini, 2015). To achieve efficient phytoremediation, two approaches can be used, namely the use of appropriate hyperaccumulator plants, proper cultivation, and growth manipulation techniques. By attempting to manipulate genetics and agronomy, the biomass of hyperaccumulator plants can be increased, as well as plants that produce a lot of biomass can increase their metal accumulation power by manipulating agronomy.

Fig. 17.11 Relations with the TF (calculated from biomass Purun tikus).

Potential of Purun tikus to restore Iron contaminated acid mine  429 Water plants that are used as bioremediation agents will accumulate metals in their bodies. The ability of plants to accumulate pollutants differs according to the type and nature of the metal to be absorbed (absorption). Aquatic plant productivity depends on the availability of resources, environmental deft, and adaptation to the environment. The order of productivity of aquatic plants from high to low is emergent plants > floating plants > submerged plants. Hyperaccumulator plants are plants that can concentrate metals in biomass at extremely high levels (Baker and Brooks, 1989). Most plants accumulate metals of 10 mg kg‑1 dry weight (BK) or equivalent to 0.001%, whereas plant hyperaccumulator metals can accumulate up to 11% BK. The metal content limit in biomass so that a plant can be called a hyperaccumulator varies depending on the type of metal. Calculation of the BCF and TF was conducted to determine the ability of Purun tikus to accumulate metal. BCF value greater than the value of the TF shows that plants would have an ability to accumulate high in iron but difficult to translocate it or the ability to metal translocate still low. The low FT value in the Fe essential metal indicates that Purun tikus uses the metal for metabolic and growth activities. Sometimes the roots also have a system of stopping metal transport to the leaves, so there is an accumulation of metal in the roots. BCF and TF factors are indicators that can distinguish the mechanism of accumulation between phytostabilization and phytoextraction. In plants that have BCF values >  1 and TF  1 and TF > 1, the mechanism that occurs is phytoextraction. In this study, the average BCF values >  1 and TF  1000 mg/kg of Ni, Pb, and Cu or > 10,000 mg/kg (dry wt.) of Zn and Mn (Baker et al., 2000). It is an eco-friendly approach and can be attained either by root colonizing microbes or by plants themselves, which convert them to nontoxic metabolites. Process of phytoremediation is influenced by various factors such as plants species, soil conditions viz.: pH, cation exchange capacity (CEC), organic matter content, etc., and also the type of metals (Xian and Shokohifard, 1989; Otte et al., 1993; Barman et al., 2001; Spinoza-Quinones et al., 2005). Based on the mechanisms of action, there may be four different plant-based technologies for metal phytoremediation: (i) phytoextraction: It involves metal absorption from the soil by the plant’s root system, thereby translocation to shoots from where they can be harvested. It is broadly used to extract metals from the contaminated site followed by recovery from plants. (ii) Phytovolatilization: Sometimes plants extract certain metals present in soil and then discharge them in atmosphere through direct volatilization (from shoot or leaf) or indirect volatilization from root. (iii) Phytostabilization: Certain metal contaminants are immobilized through the plant by binding these contaminants to soil particles, hence limiting their migration. Interactions of roots and microbes jointly perform this activity. (iv) Phytofiltration: seedlings (blastofiltration) or roots (rhizofiltration) are used to adsorb or absorb metals through water (Prasad and Freitas, 2003). Phytoremediation also has some limitations that require further research on the type of plants used for phytoremediation and related soil conditions (Danh et al., 2009). (i) It suffers from low yield and less efficiency rate as compared to any other traditional techniques viz. chemical, physical and microbiological. (ii) Sometimes the contaminants leach into aquatic system due to poor root system. (iii) The plant growth is also retarded in soils contaminated with higher concentration of toxic metals (Danh et al., 2009). (iv) In some instances, metals complexed with organic portion of soil are not bioavailable to plants, similarly sometimes, the water-soluble metals, also pass the root system without accumulation. Metal absorption capacity of soil is determined by the CEC of soil. Higher CEC means greater absorption and mobilization of metals. For example, clay-type soil hinders mobility and metals availability in soils (Zia et al., 2010). Metals present in the exchangeable soil solution are easily absorbed by plants (Meers et al., 2007). Sometimes, soil pH also affects metal uptake by roots, for example, Zn and Cd uptake in Thlaspi caerulescens showed pH-dependence (Wang et al., 2006). Bioavailability of some metals is increased in acidic soil, owing to the higher solubility of metals, as is the case for Cd (Kirkham, 2006). Likewise, multiple metal contaminations also inhibit growth of certain hyperaccumulator plant species thus demanding detailed analysis and research on specific hyperaccumulator species before application. For example,

492  Chapter 21 T. caerulescens is sensitive toward copper (Cu) toxicity, thus while using this species for remediating Cd/Zn from soils in the presence of Cu, its overall growth, particularly photosynthesis is affected (Mijovilovich et al., 2009).

21.4.2  Hyperaccumulator plants: Primary mainstay for phytomining The concept of phytomining depends largely on the selection of appropriate hyperaccumulator plant species. Generally, indigenous varieties are favored as they are acclimatized to native conditions and seasonal cycles. However, in some cases, for the extraction of specific metals, some exotic plant varieties may also be preferred (USEPA, 2000). Some specific criteria in selecting plant species for phytomining are as follows: (i) it must tolerate the level of metal present at the site. (ii) It must accumulate, translocate and uptake specific metal adequately. (iii) It should have high growth rate and biomass yield. (iv) It must tolerate extreme environmental conditions like shortage of water (drought) or standing water, and acidic/basic or saline soil. (v) The availability and preferred habitat (terrestrial, aquatic, semi-aquatic, etc.) of the plant must be considered. (vi) Its root characteristic and depth of root zone are also significant criteria. Broadly, the plant species that can survive on metal-rich soils are called metallophytes. These are further classified into three basic categories: (i) indicators: these help in the exploration of mineral deposits in soils, as they absorb proportional quantity of metals from soils. (ii) Excluders: tolerance mechanism in these are based on the exclusion of metals. (iii) Hyperaccumulators: as already mentioned above, these plants accumulate an excessive amount of toxic metals in their shoots, sometimes as high as 100 times of nonaccumulating plants (Anderson et al., 2003), which can be further extracted at an economical level. Several comprehensive reviews have summarized many important aspects of this novel green technology (Padmavathiamma and Li, 2007; Kramer, 2010). As discussed earlier, hyperaccumulators may accumulate 10–500 times higher concentration of heavy metals, as compared to nonhyperaccumulator plants (Baker and Brooks, 1989; Reeves and Baker, 2000). This property is attributed to physiological, molecular, genetic, and ecological traits. This concept was initialized by Baker et al. (1991) for Cd and Zn phytoextraction. In the previous decade, around 500 plant species were reported as hyperaccumulators, which includes, 101 families including asteraceae, cyperaceae, brassicaceae, caryophyllaceae, fabaceae, cunouniaceae, flacourtiaceae, poaceae, lamiaceae, euphobiaceae, and violaceae (Kramer, 2010). The list includes several plant species viz., Thlaspi sp. (Baker et al., 1994), Brassica sp. (Blaylock et al., 1997; Huang et al., 1997), Alyssum sp. (Kramer et al., 1996), etc. Some of them are very specific for particular metal, possess small biomass, show slow growth habit, and need careful management for growth (Gleba et al., 1999), which make them unsuitable for commercial purpose. Hence, the identification of new plant species with high biomass along with a tolerance for multiple metals is a key aspect of phytomining research. Recently, a hyperaccumulator plant Glochidion cf. sericeum (Phyllanthaceae) has been reported to accumulate 1.5 mg/g of Co

Phytomining 493 Table 21.1: List of potential hyperaccumulator plant species of metals for phytomining. Metals Ni

Pd and Pt Au

Cu, Pb, Ag, Cd, and Zn Re Tl Ge

Plant species

References

Streptanthus polygaloides Rinorea bengalensis Phyllanthus securinegoides Alyssum bertolonii Berkheya coddii Berkheya coddii Chilopsislinearis Dacuscarota Berkheya coddii Eleocharis acicularis Medicago sativa Biscutella laevigata Iberis intermedia Phalaris arundinacea

Nicks and Chambers (1995) Vaughan et al. (2017) Nemutandani et al. (2006)

Nemutandani et al. (2006) Rodriguez et al. (2007) Msuya et al. (2000) Prasad and Freitas (2003) Ha et al. (2011) Bozhkov et al. (2012) LaCoste et al. (1999) Rentsch et al. (2016)

and Ni, simultaneously, where Ni is stored inside the foliar epidermal cell, whereas Co is accumulated through extracellular mechanisms (van der Ent et al., 2018). Table 21.1 provides a list of potential hyperaccumulator plant species of various metals for phytomining. Transfer factor from soil (TFS) is a key selection criterion for the appropriate hyperaccumulator plant. It is the ratio of the concentration of metals present in soil and parts of the plant. The TFS value of ≥ 1 indicates higher metal accumulation in plant parts compared to soil (Barman et al., 2000). Based on TFS value, many macrophyte species are categorized as hyperaccumulators such as Ipomea sp. (for Cd, Mn, Cu, and Zn), Marsilea sp. and Eclipta sp. (for Fe, Cd, and Cu) (Gupta et al., 2008). Another aquatic sp. Elodea densa is reported as hyperaccumulator of Hg particularly in leaves, roots, and stems from the natural sediment contaminated with methyl mercurous chloride (CH3HgCI) (Ochiai, 1987). Likewise, Sesbania drummondii is a Pb hyperaccumulator with high biomass (Sahi et al., 2002). Twenty-six Co hyperaccumulator species that belong to the families of lamiaceae, asteraceae, fabaceae, and scrophulariaceae have been reported (Baker et al., 2000). Similarly, members of brassicaceae viz. Noccaea caerulescens (syn. T. caerulescens) showed Zn hyperaccumulation (Reeves and Baker, 2000) and Alyssum bertolonii showed Ni hyperaccumulation (Kramer, 2010). Sedum alfredii showed Cd hyperaccumulation (Deng et al., 2007). Pelargonium sp. (scented geranium) has been discovered as a multiple metal hyperaccumulator. It can accumulate and tolerate multiple metals such as Cd, Pb, and Ni and thus can continue usual metabolism (Dan et al., 2000; Krishna Raj et al., 2000). Vetiveria zizanioides can accumulate multiple metals in shoots and roots and is also considered as a good candidate for phytomining of a wide range of metals (Danh et al., 2009). Also, arsenic (As) hyperaccumulation has been reported in members of brassicaceae and pteridophytes (Ma et al., 2001; Karimi et al., 2009).

494  Chapter 21 21.4.2.1  Transgenic approach Using advanced molecular biology tools, it is possible to engineer plants suitable for phytomining by enhancing their hyperaccumulation property (Clemens et al., 2002). Genetic engineering is an approach capable of modifying plants such that they can facilitate maximum metal accumulation in above-ground biomass. Transgenic approaches have been used for phytomining of various metals (Cd, Cu, and Pb) and metalloids (As, Se) from contaminated soil by enhancing metal accumulation in the aboveground parts. This mainly involves metal transporters, better production of sulfur metabolism enzymes, and formation of metal-chelators, organic acids, phytochelatins, and metallothioneins (Kotrba et al., 2009). Some studies have reported the use of transgenics by overexpressing metal-chelating molecules such as citrate (de la Fuente et al., 1997), phytochelatins (Zhu et al., 1999a, 1999b), metallothioneins (Evans et al., 1992; Hasegawa et al., 1997), or ferritin (Goto et al., 1999), or by overexpressing metal transporter proteins (Samuelsen et al., 1998; Arazi et al., 1999; Van der Zaal et al., 1999; Curie et al., 2000; Hirschi et al., 2000). Using systemic biology approach bacterial pathways have been targeted to enhance Hg volatilization and tolerance (Rugh et al., 1996; Bizily et al., 1999, 2000). These works have been reviewed extensively (Kramer and Chardonnens, 2001; Pilon-Smits and Pilon, 2002; Clemens et al., 2002). As mentioned before the role of glutathione (GSH) in imparting metal tolerance has also been elucidated particularly by over-expressing its biosynthetic pathway genes viz. γ-glutamylcysteine synthetase (γ-ECS) and glutathione synthetase (GS) to enhance Cd tolerance and accumulation (Zhu et al., 1999a, 1999b; Sinha et al., 2013). Some works have reported enhanced phytoextraction capability in transgenic Indian mustard over-expressing GS and ECS (Banuelos et al., 2005), where transgenic plants have higher shoot metal concentrations of metals than control type but retain the same shoot biomass. The study revealed that ECS and GS concentration were 1.5-times higher for Cd, and 1.5- to 2-times higher for Zn, in transgenics than wild-type. Moreover, the ECS transgenics had 2.4 to 3 times more Cr, Pb, and Cu than wild type. Likewise, transgenic mint over-expressing γ-ECS gene was shown to tolerate Cd and Zn to concentrations as high as 100 ppm and 200 μM, respectively (Sinha et al., 2013). In general, under stressed conditions, plants have elevated levels of ACC, which is then transformed into ethylene by ACC oxidase; which causes a reduction in chlorophyll content, shoot height, and biomass. Many transgenic plants with modified ACC deaminase have shown improved growth in metal-polluted soil (Stearns et al., 2005; Grichko et al., 2000; Nie et al., 2002). Similarly, the use of plant growth-promoting bacteria that produce ACC deaminase and indole acetic acid, have also shown enhanced plant resistance to organic and inorganic contaminants (Burd et al., 1998; Mayak et al., 2004; Belimov et al., 2005; Reed et al., 2005; Reed and Glick, 2005). Transgenic plants generated to produce specific enzymes like ACC deaminases that breaks down plant ACC (precursor of ethylene) reduced metal

Phytomining 495 stress-led enhanced ethylene formation (Stearns and Glick, 2003). Farwell et al. (2006) assessed the use of transgenic canola and Pseudomonas putida (plant growth-promoting bacteria), expressing ACC deaminase, as phytoremediation approach for Ni-polluted soil. 21.4.2.2  Biomass yield: Second mainstay for phytomining Biomass production is another major determining factor for phytomining operations. Accumulation of metals has an adverse impact on biomass production of plants. In B. napus, Cd hyperaccumulation showed a negative correlation with biomass. Although the decrement was higher in root tissues than shoot, the above-ground biomass can be potentially used for Cd phytoextraction (Selvam and Wong, 2008). Similarly, decreased biomass production has been recorded in Glycine max and Phaseolus vulgaris in presence of vanadryl sulphate (VOSO4, Kaplan et al., 1990). On the contrary, accumulation of some metals such as Pb, Zn and Cd, stimulate biomass production in certain species like A. paniculata (Tang et al., 2009). The effect of metal appears to be dependent on concentration and duration of metal exposure. For example, E. fluctuans can tolerate up to 13.7 μM of vanadium pentaoxide, however, beyond 44.8 μM the plant showed significantly reduced biomass (approximately by 42.47%) and even toxic responses during increased treatment duration (Sarma et al., 2009). Likewise, Cr toxicity is also observed with increasing time duration in Vallisneria spiralis L., where 0.1 μg mL−  1 Cr led to 7% decline in biomass after 48 h and 64% after 72 h of treatment with 10 μg mL−  1 Cr (Vajpayee et al., 2001). Recent approaches are employing transgenic technologies for raising biomass yield of plants to modify tolerance, uptake, or homeostasis of trace elements (Kramer and Chardonnens, 2001). In an attempt to increase agronomy of A. murale species, used for phytomining Ni ultramafic areas, the different combinations of fertilizers and harvesting time were optimized to achieve maximum biomass yield (0.3 to 9 t/ ha). It was also observed that cropping A. murale plantlets were more beneficial than native plants. The total Ni extraction was nearly 1.7 to 105 kg/ha (Bani et al., 2015). Many studies have targeted techniques to enhance Cd phytomining by increasing the harvestable yield of hyperaccumulator crops. They suggested the use of monocot herbicides in the field to end the competition and promote the growth of N. caerulescens (Simmons et al., 2015; Broadhurst et al., 2015; Nkrumah et al., 2016). Without the application of these herbicides, the biomass is harvested in very low density and the minimal amount of Zn and Cd, which questions the efficiency of phytomining (Ernst, 2005; Robinson et al., 2015).

21.5  Economical aspects of phytomining Phytomining requires solar energy that generates bio-ore, which is nearly sulfur-free. The metals are extracted from these bio-ores by various chemical techniques such as roasting (i.e., burning of plants), sintering, or smelting followed by acid dissolution and electrowinning (Robinson et al., 1999). These bio-ores require less energy during

496  Chapter 21 smelting and have higher metal content than their traditional counterparts; also, they can be held least responsible for acid rains (Anderson et al., 1999b; Brooks et al., 1998). Thus, it is cheaper than conventional techniques, however, it requires a much longer time duration; however, yet it is possible to harvest some metals from sub-economic ore bodies or metal-contaminated mining sites at an economical level (Anderson et al., 2003). According to Chaney and Baklanov (2017), some metals such as Cd have little or almost no economic value, while others such as Zn and Mn can be used as fertilizers and Ni and Au have obvious economic values. The most determining factor of phytomining is the worldwide price of phytomined metals (Brooks and Robinson, 1998; Harris et al., 2009), thus the most preferred metals for phytomining are Au, Tl, Co, and Ni owing to their high market prices and metal concentrations. Although the price of certain metals such as U and Au is high, the concentration of these in hyperaccumulator plants viz. A. confertifolia and B. coddii is 100 and 10 mg/kg, respectively, and the resulting biomass is also low viz. 10,000, 20,000 kg/ ha. Owing to their low biomass the idea turns out to be uneconomical (Mahar et al., 2016; Sheoran et al., 2009). So, identification of good hyperaccumulators with high biomass is necessary for phytomining. Phytomining of Mn is considered as more economical as the net concentration of metal in plant Macadamia neurophylla is quite high, nearly 1650 mg/kg, making it more profitable (Jaffre, 1980). To enhance the economy of phytomining of certain metals such as Pt and Pb, chelators viz. EDTA may be added to enhance their accumulation. EDTA increased Pb transport into the xylem and enhanced the translocation of Pb from roots to shoots (Huang et al., 1997). The economic aspects and present scenario of phytomining for some leading metals are discussed below: Nickel (Ni): Due to large commercial demand, Ni phytomining has received the utmost attention. It has been tested in the land area containing Ni-rich soils and Ni hyperaccumulator plants (Bani et al., 2015; Li et al., 2003; Nkrumah et al., 2016). Phytomining technique was pioneered in Ni using hyperaccumulator plant Streptanthus polygaloides which yields nearly 100 kg/ha S-free Ni (Nicks and Chambers, 1995). Likewise, hyperaccumulation of Ni is evaluated on two other plant species A. bertolonii from Italy and B. coddii from South Africa. It was shown to accumulate upto 20,000 mg Ni/kg dry weight and 10,000 kg biomass/ha can be achieved per year (Chaney et al., 2007). It was also shown that by using different combinations of N and P fertilizers, the biomass of the plant can be enhanced threefold (4.5 t/ha to 12 t/ha) without affecting Ni accumulation (7.6 g/kg) (Robinson et al., 1997). Another species A. serpylli folium had shown hyper-accumulation of Ni present in ultramafic areas of Portugal (Alves et al., 2019). Another approach for Ni phytomining was elaborated in Rinorea bengalensis and Phyllanthus securinegoides, where bio-ore was initially washed with water for K recovery, followed by leaching with sulfuric acid and extraction of Ni as hydroxide salts [Ni(OH)2]. The

Phytomining 497 metal can then be harvested using potassium carbonate solutions. The by-products: K-solution and gypsum (CaSO4.2H2O), so raised could be used as fertilizers too (Vaughan et al., 2017). Gold (Au): Application of phytomining for harvesting gold has larger applications at artisanal and small-scale gold mining (ASGM) location. This can generate revenue and help in rehabilitation (Wilson-Corral et al., 2011). However, the major concern is the extraction of metals from plants. Various combinations of approaches have been used and reported to enhance the recovery of gold. In a method reported by Krisnayanti et al. (2016), tobacco plants were grown in soils with gold concentration (1 mg/kg). The plots were watered with sodium cyanide (NaCN) to induce metal uptake and plants were harvested. Around 100 kg of biomass was harvested, air-dried, and ashed. To this ash, silver and borax were added as collector metal and smelting was done at high temperature for metal extraction, however, the final gold yield was still low about 1.2 mg Au/kg dry wt. biomass suggesting need to have more thrust on this area. Gold phytomining might be more profitable in case soils are ground and kept on a plastic liner to gather any leaching cyanide required for dissolution and hence uptake of gold (Anderson et al., 1999a). B. coddii, Daucus carota and Brassica juncea are reported to accumulate as much as 20 mg/kg of gold whereas B. juncea can accumulate up to 57 mg/kg of gold after ammonium thiocyanate supplementation (Anderson et al., 1999a; Prasad and Freitas, 2003). In 2017, another report on gold accumulation was reported in dessert willow plant Chilopsis linearis. It was observed that plants can survive on as high as 320 mg/L of Au concentrations added in agar-based media, along with an increase in gold concentration in plants with aging. The X-ray absorption spectroscopy data suggested the formation of gold nanoparticles in plant tissues, whose size was dependent on Au concentration and location. Gold nanoparticles have huge potential in nanotechnology industries (Reeves and Baker, 2000; Gardea-Torresdey et al., 2005; Harris and Bali, 2008). Thallium (Tl): Although the demand for Tl is less, phytomining offers enough economic return for it to be profitable (Brooks et al., 1999). Both Biscutella laevigata and Iberis intermedia were reported to accumulate very high concentrations of Tl (1.94% and 0.4%, respectively) in their above-ground plant parts (LaCoste et al., 1999). Phytomining of Tl from plant species Iberis intermedia (Brassicaceae) showed accumulation up to 3.07 mg/g (0.31%) of Tl in its dry matter. It also showed tolerance to up to 2 mg/g Tl in soil. It is estimated that three crops of this plant are enough to detoxify soils containing 10 μg/g of Tl with the production of bio-ore containing 0.08% of Tl in dry matter. It is anticipated that the biomass yield of 10 t/ha could generate revenue of approximately $1200/ha., however, the project requires a large landscape, thus challenging its feasibility (Leblanc et al., 1999). In a pot experiment, LaCoste et al. (2001) observed maximum thallium level nearly 400 mg/kg (dry matter) in Iberis and suggested that it would take five sequential cropping of Ibera to reduce 1 mg Tl/kg to 0.1 mg Tl/kg in the soil. Anderson et al. (2005) reported that ligand like EDTA is required to induce phytoextraction which makes this technology difficult as permission is required to conduct it.

498  Chapter 21 Germanium (Ge): Another important heavy metal, germanium (Ge) is mostly recovered as a by-product from zinc mines. Phytomining offers the possibility of Ge recovery using hyperaccumulator plants. The demand for Ge has increased tremendously due to its use in fiber optics (40%) because of the high refractive index and low optical dispersion. The Ge production was 153 t in 2013 and according to a market study of Merchant Research and Consulting Ltd (2014), the global demand for Ge will amount to 270 t in 2030. Considering the increasing demand for Ge, “PhytoGerm” program was launched by German Federal Ministry of Education and Research which concentrates on alternative methods for mining and extracting of Ge. The potential hyperaccumulator species of Ge is Phalarisar undinacea (ribbon grass) which can accumulate Ge from soils such as mine tailings. Rentsch et al., 2016 have analyzed the economic pre-feasibility of this program and suggested that the extraction process of Ge needs to be refined, and the PhytoGerm method was preferred. In brief, it is based on the leaching and distilling of Ge with HCl. Ge is extracted as GeCl4. This is injected into the second reactor with NaOH such that germanium (IV)-oxide is precipitated, which is separated by filtration. It was estimated that production of 3.9 kg of germanium (IV)-oxide can be achieved per year. This process also offers the probability of extracting valuable by-products like phosphate (Rentsch et al., 2016).

21.6  Multi-benefit nature of phytomining Plants provide several ecosystem services such as cleaning of air, soil, and water, improvement of the hydrological cycles, nutrient cycles, etc. Phytomining is a natural process and done through the cultivation of green plants. The same plant improves/restores the soil quality parameters along with the reduction of hazardous substances from the soil and carbon dioxide which is considered as a major greenhouse gas from the atmosphere through carbon sequestration. Phytomining provides diverse benefits including environmental, economic, societal, and employment generation (Fig. 21.4). The majority of plants have been reported to enhance soil microbial diversity and induce the microbial enzymatic activities in their presence. Plants improve the nutrient level in the soil along with other soil quality indicators such as water-holding capacity, organic content, etc. The production of energy from biomass is one of the important practices in the field of bioenergy (McKendry, 2002a, 2002b; Balat and Ayar, 2003). During the process of incineration, the produced energy (bioenergy) may be utilized in many ways, e.g., production of electricity, thermal energy, etc. (Mirza et al., 2008). This process makes phytomining an economically viable method. Cultivation of plants enhance the aesthetic values in the society and thereby, increase societal development.

Phytomining 499

Fig. 21.4 Multi-benefits of phytomining.

21.7  Limitations of phytomining Although phytomining is an eco-friendly and cheaper method of satisfying greater demand of metal through hyperaccumulator plants, the process is limited by various factors such as the need for an extended time duration, large contaminated site, specific accumulation of target metal from a mixture of metals in the above-ground part. Low biomass or slow growth due to metal toxicity, climatic condition, loss to biodiversity, entry of metals in food chain, application of chelates, exudates release nonoptimal soil moisture and pH are also some of the problems associated with phytomining (Bhargava et al., 2012; Ali et al., 2013; Mahar et al., 2016).

21.8 Conclusions Among the available conventional mining methods to extract the essentials metals from ores or recovery of valuable metals from the residues, phytomining has several advantages. It offers the possibility of exploiting ore or mineralized soils that are otherwise uneconomic to work with. Selection of appropriate plant species, which can accumulate significantly high amount of metals is one of the important aspects of phytomining. Hyperaccumulator plants have excellent efficiency to extract high level of metals without exhibiting any toxic effect, and these plants are considered as most suitable candidates for phytomining. Phytomining also offers several other benefits like it enhances soil quality, causes carbon sequestration, generates employment and thereby leads to capital gain and societal development.

500  Chapter 21

Acknowledgments RS acknowledges DBT-BioCARe project no. BT/PR30922/BIC/101/1184/2018 funded by DBT, India for financial support. PS acknowledges DST-SERB project no. ECR/2016/000888 and UGC-Start-up grant no. F.45(107-FRP)/2014(BSR) for financial support. KB is thankful to Science and Engineering Research Board (SERB), New Delhi, India for the award of research grant (EEQ/2017/000476).

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Index Note: Page numbers followed by f indicate figures and t indicate tables. A ACC deaminase, 494–495 Acetic acid, 70–71 Acid mine discharge (AMD), 90 Acid mine drainage (AMD), 62–63, 120–121, 168–169, 377–378, 378f, 409 abatement technique, 181–182 fly ash, treatment with, 175–183 Acidogenesis, 70–71 Acid rock drainage (ARD), 91–92 Adesmia atacamensis, 138–142, 140–141f Agro-mining, 21 Agrostis capillaris, phytostabilization, 388 Agrostis tenuis, phytostabilization, 388 Air contamination mining activity, impact of, 92 Algae, 105–106 Algal bloom, 4–5 Algal strains collection and characterization of, 107 in fly ash polluted water bodies distribution and dominance, 109, 110t heavy metal accumulation, 109–110, 111t physicochemical properties, 108–109, 108t Alyssum sp., phytoextraction, 389–390 Amendments, 129–136 American Coal Ash Association (ACAA), 173 Anaerobic fermentation, 73

Animals, heavy metals (HMs) toxicity on, 8 Anthropogenic processes, 6 Antioxidant defense systems, 364 Arbuscular mycorrhizal fungi (AMF), 131, 134 activated in roots of A. nummularia, 134, 135f in backfill soil, 134, 134f Arid environment, mine tailings phytoremediation of, 123–127 endemic and native species in mining areas in, 127–129 limitations, 156–158 Arsenic (As), 380–381 hyperaccumulation, 493 phytoremediation, 395–397t, 398 phytotoxicity, 386 Arsenolite, 380–381 Arsenopyrite, 380–381 Arundo donax, 296 Ascorbate, 365 Astragalus bisulcatus, 390–391 Astragalus racemosus, 389–390 Atriplex halimus, 276 Atriplex nummularia, 136, 137f, 143–146, 144–147f Autochthones plants, 127 Avena sativa, 123 Azadirachta indica, 68–69 Azeotropic distillation, 75

B Babool. See Vachellia nilotica Bamboo diversity, 444 environmental and socioeconomic benefits, 443

507

plantation, 447 protection, 447 selection of sites, 444–445, 445f selection of species, 445–446, 446t soil carbon sequestration, 443–444 sustainable biodiversity, 442–443 for sustainable development and climate change, 448 uses, 447–448 Barley. See Hordeum vulgare Bauxite, mining, 91 BCF. See Bioconcentration factor (BCF) Berkheya coddii, 398 Bioaccumulation, metal, 360 Bio-augmentation, 189–190 Bioavailability, 383, 491–492 Bioconcentration factor (BCF), 141–142, 149, 155, 156f iron accumulation, 427, 429 Bioenergy crops, 57–66, 61t production, 70–73, 71f Biomass, 70 bioenergy conversion, 70–71 Bio-oil, 72–73 Bio-ore, 489, 495–496 Bioremediation, 228 Bitumen, 90–91 Blue-green algae (BGA), 105–106 Bottom ashes, 73–74 Brachiariabrizantha grasses, 475–476 Brassica juncea phytoextraction, 389–390 phytostabilization, 388 phytovolatilization, 390–391 rhizofiltration, 392

Index Brassica napus L., 123 Buffelgrass. See Cenchrus ciliaris L.

C Cadmium (Cd) accumulation, 15 hyperaccumulation, Sedum alfredii, 493 phytoremediation, 395–397t, 398 phytotoxicity, 386 toxicity, 381 Calcium carbonate (CaCO3), from eggshells, 133, 133f Carex hirta L., 465 Caribbean stylo. See Stylosanthes hamata Carotenoid, 16 Castor Bean. See Ricinus communis Castor plant, 263–264 Cation diffusion facilitator (CDF), 20 CCP. See Coal combustion products (CCP) Cellulolytic enzymes, 72 Cellulose, 70–71 Cenchrus ciliaris L., 352 Chelate rings, 419 Chelators, 208, 214 application, 214–216 Chemical remediation encapsulation, 40 immobilization, 39 soil washing, 40 Chile, 115 mine tailings, 120–122 mining activity in, 120–122 Chloride, 108–109 Chlorpyrifos, 64 Chromium toxicity, 209–213, 209–213f Citrate, 494–495 Citronella grass. See Cymbopogon citratus Clay fraction, 384 CMZ tailings A. atacamensis, 138–139, 140f, 142, 142f alfalfa in, 138–139, 139f A. nummularia, 136, 137f, 144, 144–147f, 146

drip irrigation of transplanted species in situ, 138, 139f G. rigens, 149–150, 150–152f P. hortorum, 151, 151–152f P. tamarugo, 136, 137f, 147–149, 148–149f S. molle, 152–156, 153–154f Coal ash, utilization for mine reclamation, 176–177 Coal combustion products (CCP), 173–176 Coal fly ash, 172–175 Coal mine degraded land plant species selection, 338–341, 342t reclamation (see Reclamation) revegetation, 333–335, 341–352, 343f fruit tree species, 349–350 grasses species, 350–352, 351f grass-legume cover, 347–348, 348f indigenous vs. exotic species, 347 legume, 348–349, 349t role, 335–338, 337t shrub and medium-size plant species, 349, 350f trees, 343, 344f, 345–346t soil organic carbon, 325–326, 326f vegetation, development methods, 327 Coal mining, 89–90 activities, 409 Cold pressing, 75 Constructed wetland (CW) system, 410 in Indonesia, 410 plant, 410 purun tikus (Eleocharis dulcis) acid mine drainage, 415 batch flow system, 415 batch system, 415 continuous flow system, 415 HSSF-CW, 415–416 operational factor, 415 performance, 414 role of, 416–420, 417f seedlings, planting space, and growth in, 420–423, 421f

508

vertical downward flow type, 416 VSSFCW, 415–416 Contaminants accumulation and translocation into aerial parts, 13–15 environmental, 4–5, 5f plant soil interaction and bioactivation of, 12–13 tolerance in plants, 15–17 types of, 458 Contamination environmental, 4–5, 5f level of, 459–460 Continuous phytoextraction, 389 Copper, 115 mining, 91–92 phytoremediation, 394, 395–397t phytotoxicity, 386 toxicity, 381 Crassulacean acid metabolism (CAM), 62 Crude oil, 90–91, 455–456 components in, 458 Zea mays in removal of, 458–460 Cyclodextrins, 18 Cymbopogon citratus, 350–351 Cyprus rotundus, 462

D Decontamination, of soil, 36–37, 37f Degraded lands. See Land degradation Detoxification, 15–16 Dioxane, 64 Drilling, 170–171 environmental impacts of, 170–172

E Echinacea elongatus, 465 Echinacea purpurea, 463–466 Eclipta sp., 493 Eco-rejuvenation technology (ERT), bamboo diversity, 444 environmental and socioeconomic benefits, 443 plantation, 447 protection, 447

Index selection of sites, 444–445, 445f selection of species, 445–446, 446t soil carbon sequestration, 443–444 sustainable biodiversity, 442–443 for sustainable development and climate change, 448 uses, 447–448 Ecorestoration, 185–188 Egtazic acid (EGTA), 69–70 Electrokinetic remediation, 39 Electrokinetic treatment, 9 Elements, 373 Elephant grass, 65 Elodea densa, 493 Encapsulation, 40 Enhanced rhizosphere biodegradation (EPA). See Phytostimulation Environmental contamination, 4–5, 5f Environmental safety, 473 Enzymatic antioxidants, 364 Epilobium dodonaei, 362–363 Essential oil, 215–216 extraction, 75–76 Exchangeable fractions, 383 Excluders, 492 Ex-tin mining catchment, 241–243

F Faba bona Medic., 465 Ferric hydroxide, 381 Ferritin, 494–495 Fertilization, 462 Festuca rubra, phytostabilization, 388 FGD. See Flue-gas desulfurization (FGD) First-generation bioenergy crops (FGECs), 62 Flavonoids, metal detoxification, 365 Flue-gas desulfurization (FGD), 173–174, 180–183 Fluidized bed combustion (FBC), 173–174, 181 Fly ash (FA), 73–74, 105, 167, 173–174 filling underground mines with, 177–181

phytoremediation of, 183–193 phytorestoration, challenges and opportunities in, 195–198 for surface mining, 181–183 Forest reclamation, on abandoned mines, 188–191 Forestry Reclamation Approach (FRA), 188, 195–197 Fossil fuels, 60–61 Fracking, 171–172, 473, 477–478, 480

G γ-glutamylcysteine synthetase (g-ECS), 494–495 Gas chromatography-mass spectrometry (GC-MS), 461 Gazania rigens, 149–150, 150–152f Genetic engineering, 494–495 Geophysical mapping technique (GPS), 181–182 Germanium (Ge), 74 phytomining, 498 Giant reed. See Arundo donax Glutathione (GSH), heavy metal detoxification, 365 Glutathione synthetase (GS), 494–495 Gold (Au) environmental pollution sources, 374 acid mine drainage, 377–378, 378f open pits, 374, 375f tailings and waste rock, 375–377, 377f underground mine, 374–375, 376f heavy metal toxicity, 380–387 arsenic, 380–381 cadmium, 381 copper, 381 lead, 382 mercury, 382 phytodegradation, 392–393 phytostimulation, 392 zinc, 382 phytomining, 497 phytoremediation, 394–398, 395–397t

509

soil and sediments pollution, 379–380 water pollution, 378–379 Grasses, 186–187 Green algae (GA), 105–106 Greenhouse gases (GHGs), 167

H Hazards biological, 94–95 chemical, 94–95 physical, 94–95 Heavy metals (HMs), 4–5, 33–34, 219, 373 accumulation and plant growth, 361–363 cell wall sequestration of, 16–17 contaminants sources and pathways, 225 contamination of, 95–96 decontamination of, 373 detoxification, 16–17 extraction of, 73–74 in gold mine environment, 380–387 phytoavailability, factors affecting, 383–385 phytotoxicity, 385–387 properties, 380–382 occurrence and mechanisms, 223–225, 223t impact of, 224–225, 224t phytoremediation, 19, 229–240, 394–398, 395–397t plants stress defense mechanisms, 363–366 toxic effect on, 361, 361t sources of, 5–6 anthropogenic, 6, 6f natural, 6, 6f sources of pollution, 36–37, 37f toxicity to animals, 8 to plants, 7–8 Hemicellulases, 72 Hordeum vulgare, 123 Horizontal subsurface constructed wetland (HSSF-CW), 415–416 Hydrodiffusion, 75

Index Hydrogen sulfide (H2S), 89 Hyperaccumulation, 490–491 Hyperaccumulators, 13f, 14–15, 34–35, 42, 184–185, 220, 488, 492–495, 493t biomass production, 495 transgenic approach, 494–495

I Immobilization, 39 Impatiens balsamina, 458 Indicators, 492 Induced/chelated-assisted phytoextraction, 389 Industrialization, 249–250 International Energy Agency, 60–61 Invasive species geographical distribution and ecology, 288–290 phytoremediation, 290–293, 291f classification, 290, 291f importance, 293–298, 295t metal hyperaccumulation, 290 phytoextraction, 292–293 phytofiltration, 292 phytostabilization, 291 phytotransformation, 293 phytovolatilization, 292 Ipomea sp., 493 Ipomoea carnea, Cd phytoextraction, 398 Iron accumulation bioconcentration factor, 427, 429 hyperaccumulator plants, 429 iron-plaque stability, 429–430, 430f phytochelatin detoxifies plants, 423 phytoremediation, 426–427 plant mechanism, 429 plants wetlands, 425 polynomial equation, 424 SSFCW, 424 translocation factor, 427–428, 427–428f transporter proteins, 425 VSSFCW system and HSSFCW system, 424, 424f Iron ore mining, 91 Iron regulated transporter 1(IRT1), 15

J Jatropha, 65–66

K Khus Grass. See Vetiveria zizanioides

L Land degradation, 439 biodiversity, 441–442 causes of, 440 climate change, 440–441 eco-rejuvenation technology (see Eco-rejuvenation technology) in India, 440f mining activities impacts, 440–441, 442f Lead hyperaccumulator, Sesbania drummondii, 493 phytoremediation, 394–397, 395–397t phytotoxicity, 386 toxicity, 382 Legacy mine tailings, 307–308 Legumes, 186–187 Lemongrass, 208–209. See also Cymbopogon citratus Life cycle analysis, 480 Lolium perenne, 128–129

M Malondialdehyde (MDA), heavy metal detoxification, 365 Manganese, mining, 91–92 Marsilea sp., 493 Medicago lupulina L., 465 Melilotus sp., 153–154, 154–155f Mercury (Hg), 44 phytoremediation, 395–397t, 398 phytotoxicity, 387 toxicity, 382 Metal accumulation, 15, 66 accumulator plants, 13f, 14 bioavailability, 383 chelator, 20 excluder plants, 13–14, 13f, 361t hyperaccumulator plants, 66–67

510

indicator plants, 14 sequestration, 20 Metallophytes, 359–360, 492 Metallothioneins, 365, 494–495 Metal ore, 307 Metal tolerance/transport protein (MTP), 20 Methane, 73 Methanogenesis, 70–71 Methyl isobutyl ketone (MIBK), 74 Microbial activity, 44 Microbial biomass, 135–136 Microwave-assisted extraction (MAE), 75–76 Microwave-assisted hydrodistillation (MAH), 75–76 Microwave hydrodiffusion and gravity (MHG), 75–76 Mineral and Petroleum Resources Development Act (MPRDA), 479 Mineral oil, 90–91 Mine soil, 330 Mine spoil, 330 phytoremediation, 226–228 bioremediation, 228 phytodegradation, 227 phytoextraction, 226–227 phytostabilization, 227 phytostimulation and transformation, 228 phytovolatization, 227 rhizofiltration, 227 vetiver grass, 228 tin mining sites, 228–229, 230–238t weathering atmospheric dispersion, 226 fluvial dispersion, 225 gravitational dispersion, 226 Mine tailing, 36–37, 115–116, 229 chemical characterization after metals treatments, 155–156, 157f chemical stabilization, 308–309 and environment, 309–310 legacy, 307–308 physical and chemical characteristics, 277 physical techniques, 308–309 physicochemical properties, 119

Index phytoextraction, 126 phytoremediation amendment on tailing availability, 129–136 arid and semiarid environment, 123–129, 156–158 assessment, 136–156 phytostabilization, 308–309 acidic, 318 growth of metallophytes, 310–312 mechanism, 311f microorganism community role, 314–316 mine ecosystem restoration, 310–316 plant selection, 316–317 reclamation, 318–319 rehabilitation, 318 soil substrate, 312–314 phytostabilization of, 118, 126 remediation, 119 restoration of vegetation, 277 Mining, 249–250, 487 bauxite, 91 coal, 89–90 contaminant effects on air, 92 on human beings, 94–96 on plants, 94, 96t on soil and soil microorganism, 94, 95t on water, 92–93, 93t copper and manganese, 91–92 environmental impacts of, 170–172 iron ore, 91 problems related to, 88, 88f social impact of, 96–97 surface, 170–171 underground, 170–171 uranium, 92 Mining dumpsites sulfide minerals, 89 type and characteristics of, 88–92 Mining Environmental Liabilities (MEL), 116–117 Mining methods, on soil, 222–223 Mining waste, 219, 287–288 composition of, 222

Ministry of Environment, Forest and Climate Change (MoEF&CC), 197 Mirabilis jalapa, 69–70 Miscanthus spp., 62–63 Multidrug and toxic compound extrusion (MATE), 20 Multistress tolerance, 465–466

N Naphthenic acids, 463–464 National Development Plan (NDP), 479 National Thermal Power Corporation (NTPC), 106–107 Natural gas, 478 Neem. See Azadirachta indica Nickel, phytomining, 496–497 Nicotianamine, 19–20 Nitrogen fertilizer, 186–187 Noccaea caerulescens, Zn hyperaccumulator, 493 Nonenzymatic antioxidant systems, 364–365 Nonprotein thiol (NPT), metal detoxification, 365 Nuclear energy, 249 Nutgrass. See Cyprus rotundus

O Oats. See Avena sativa Ocimum basilicum, 69 Oil drilling, 171–172 Oil drilling sites (ODS) abandoned, phytoremediation of, 474–476 characteristics of, 456–457 petroleum hydrocarbons, 455–457 phytoremediation, 457–458 factors influencing, 458–460 plant species, selection of, 460–466 Open-pit mines, 374, 375f Organic pollutants, 4–5 Organic xenobiotics, 4–5 Ornamental plants, 59, 69–70 Orpiment, 380–381 Over burden soil (OBS)

511

chelate and metal-assisted phytoextraction, 213–216, 214–215t, 216f physicochemical properties, 208 Oxidative stress, 130

P Pelargonium sp., 493 Pennisetum pedicellatum Trin., 351–352 Persistent organic pollutants (POPs), 4–5 Petroleum, 455–456 auxin, 463–464 contaminants, plant species using for phytoremediation of, 458, 459t Petroleum hydrocarbons (PHCs), 455–457 Impatiens balsamina in removal of, 458 Phalaris arundinacea, 74 Phalarisar undinacea, 498 Phosphorus, 413 Phragmites australis, 359–360 Phyllanthus securinegoides, 496–497 Physical remediation electrokinetic remediation, 39 soil isolation, 38–39 soil replacement, 38 soil vitrification, 39 Phytoavailability, 383 Phytocap, 185–188 Phytochelatins, 365, 494–495 Phytocover, construction of, 183–193 Phytodegradation, 11, 11f, 185, 227, 392–393 in mine areas, 45 Phytoextraction, 9–10, 73–74, 184–185, 226–227, 275, 292–293, 388–389, 457–458 advantages and limitations, 389 in arid environment, 43 Brassica juncea, 389–390 disadvantage, 389 invasive species, 292–293 in mine areas, 42–43 mine spoil, 226–227

Index Phytoextraction (Continued) mine tailing, 126 plants used, 389–390 in temperate environments, 42 Phytofiltration, 292. See also Rhizofiltration PhytoGerm, 74, 498 Phytomining, 21–22, 22f, 59, 126–127, 487 beneficial aspect, 490–492 concept of, 488 concerns associated with, 490–491, 490f economic aspects, 495–496 germanium, 498 gold (Au), 497 nickel, 496–497 thallium, 497 hyperaccumulator plants, 492–495, 493t biomass production, 495 transgenic approach, 494–495 limitations, 499 multi-benefits, 498, 499f process of, 489, 489f prospects of, 488–489, 488f using B. coddii, 66–67 Phytoplanktons, 105–106 Phytoremediation, 3–4, 9–11, 57–59, 118, 207, 374, 399, 456, 473, 487 of abandoned mining areas, 41–45 of abandoned oil drilling sites, 474–476 advantages and limitations, 398–399 application, 219–220 contaminants accumulation and translocation into aerial parts, 13–15 plant soil interaction and bioactivation of, 12–13 tolerance in plants, 15–17 definition, 387 energy plants potential in, 47 of fly ash treated mine site, 183–193 heavy metals, 394–398 invasive species, 290–293, 291f classification, 290, 291f importance, 293–298, 295t

metal hyperaccumulation, 290 phytoextraction, 292–293 phytofiltration, 292 phytostabilization, 291 phytotransformation, 293 phytovolatilization, 292 iron accumulation, 426–427 mechanisms of, 10f, 12–15 metal accumulation and translocation, 15 mine spoils, 226–228 bioremediation, 228 phytodegradation, 227 phytoextraction, 226–227 phytostabilization, 227 phytostimulation and transformation, 228 phytovolatization, 227 rhizofiltration, 227 vetiver grass, 228 of mine tailings amendment on tailing availability, 129–136 in arid and semiarid environment, 123–127 assessment, 136–156 endemic and native species in mining areas, 127–129 limitations, 156–158 of ODS, plants species selection dense and deep root system, 461–463 high biomass, 461 multistress tolerance, 465–466 physiological and biochemical responses, 463–465 phytodegradation, 11, 11f phytoextraction, 9–10 phytomining, 21–22, 22f phytostabilization, 10 phytovolatilization, 10 plant selection, 393–394 rhizofiltration, 11 of toxicants, 17–20 transgenic approaches in, 45–47, 46t types of, 184–185 using plants with economic benefits, 60–70, 60f aromatic and medicinal plants, 67–69

512

bioenergy crops, 60–66, 61t metal hyperaccumulator plants, 66–67 ornamental plants, 69–70 Phytoremediator plants aromatic and medicinal plants, 67–69 bioenergy crops, 60–66, 61t biomass utilization, after harvesting bioenergy production, 70–73, 71f essential oil extraction, 75–76 heavy metals, extraction of, 73–74 metal hyperaccumulator plants, 66–67 ornamental plants, 69–70 Phytostabilization, 10, 43–44, 118, 124, 185, 207, 227, 275, 291, 387, 457–458 advantages and limitations, 388 in mine areas, 43–44 mine tailings, 308–309 acidic, 318 growth of metallophytes, 310–312 mechanism, 311f microorganism community role, 314–316 mine ecosystem restoration, 310–316 plant selection, 316–317 reclamation, 318–319 rehabilitation, 318 soil substrate, 312–314 plants used, 388 Phytostimulation, 228, 275, 392, 457–458 Phytotechnology, 34 Phytotoxicity, heavy metals, 385–387 Phytotransformation, 185, 227, 293, 457–458 Phytovolatilization, 10, 185, 275, 292, 390, 457–458 advantages and limitations, 390 in mine areas, 44 plants used, 390–391 Phytovolatization, 227 Pinus sylvestris, 360

Index Piptatherum miliaceum, 128 Pistia stratiotes, 296 Plant growth promoting rhizobacteria (PGPR), 189–190 Plants aromatic and medicinal, 67–69 contaminant tolerance in, 15–17 heavy metals toxicity on, 7–8 hyperaccumulator, 13f, 14–15 metal accumulator, 13f, 14 metal excluder, 13–14, 13f, 361t metal hyperaccumulator, 66–67 metal indicator, 14 metal localization, 360 mining activity, impact of, 94, 96t ornamental, 69–70 revegetation and survey in mining areas, 40–41 soil interaction and bioactivation of contaminants, 12–13 species selection for phytoremediation of ODS dense and deep root system, 461–463 high biomass, 461 multistress tolerance, 465–466 physiological and biochemical responses, 463–465 Pollutants, 4–5 Pollution, 3 Polycyclic aromatic hydrocarbons (PAHs), 15–16 Zea mays-Streptomyces in removal of, 458 Polypogon australis, 128–129 Poplars. See Populus spp. Populus spp., 63–64 Pre-fracturing injection, 480–481 Progenies, 250 Proline, 364–365 Pseudomonas putida, 494–495 Pteris vittata, arsenic translocation, 398 Purun tikus (Eleocharis dulcis) constructed wetland acid mine drainage, 415 batch flow system, 415 batch system, 415

continuous flow system, 415 HSSF-CW, 415–416 operational factor, 415 performance, 414 role of, 416–420, 417f seedlings, planting space, and growth in, 420–423, 421f vertical downward flow type, 416 VSSFCW, 415–416 factors affecting, 430–433, 431–433f geography and ecology, 411–414, 411f habitat, 412 for iron accumulation, 423–430, 424–428f, 430f nutrients, 413–414 utilization, 412–413 in wetlands, 410–411 Pyrolysis, 72–73

R Radioactive substances, 4–5 Rapeseed. See Brassica napus L. Reactive oxygen species (ROS), 16, 210, 465 Realgar, 380–381 Reclamation, 287–288 of abandoned mines, 193–195 five phases, 327, 328f geomorphic reshaping, 327 hydrological stability, 329 landscape rebuilding, 329 post, 191–193 selection of plant species, 335–338, 337t soil reconstruction, 328–329 surface coal mining, 329–333 ecological restoration approaches, 330–333, 331f landscape and aesthetics, 329–330 philosophies of revegetation, 333 revegetation program, 333–335 role of vegetation, 335–338, 337t terminologies, 329–330 vegetation restoration, 329

513

Redox potential, 384 Remediation, of abandoned mining areas, 36–40 chemical encapsulation, 40 immobilization, 39 soil washing, 40 physical electrokinetic remediation, 39 soil isolation, 38–39 soil replacement, 38 soil vitrification, 39 Remediation, of tailings cover, 255–256 Renewable energy sources (RES), 35 Revegetation, 341 fruit tree species, 349–350 grasses species, 350–352, 351f grass-legume cover, 347–348, 348f indigenous vs. exotic species, 347 legume, 348–349, 349t shrub and medium-size plant species, 349, 350f trees, 343, 344f, 345–346t Rhizobacteria, 131, 189–190 Rhizodegradation, 227. See also Phytostimulation in mine areas, 45 Rhizofiltration, 11, 227, 419 advantages and limitations, 391 definition, 391 plants used, 392 Rhizoremediation, 463 Rhizosphere, 131 Ricinus communis, 65 economic importance, 267 genetics, 265–267 geography and ecology, 263–264 heavy metals causes and consequences, 268–269 oxidation and influence, 270–272 toxic impacts, 272–273 industrial values, 267–268 morphology and physiology, 264–265, 265–266f

Index Ricinus communis (Continued) phytoremediation, 273–275 application, 277–278 suitable plant, 275–277 production of oil, 267–268 Rinorea bengalensis, 496–497 Rosia Montana gold mine acid mine drainage, 378, 378f ancient gold mining traces, 377f open-pit, 375f underground excavations, 376f

S Salix spp., 62–63, 359–360 Scarification method, 75 Scirpus maritimus, 359–360 Second-generation bioenergy crop (SGECs), 62 Sedum alfredii, Cd hyperaccumulation, 493 Selenite, 390–391 Selenium (Se), 44, 272, 390–391 Semiarid environment, mine tailings phytoremediation of, 123–127 endemic and native species in mining areas in, 127–129 limitations, 156–158 Sesbania drummondii, Pb hyperaccumulator, 493 Setaria viridis, 359–360 Short-rotation woody crops (SRWC), 63–64 Silene vulgaris, phytostabilization, 388 Silybum marianum, 128 Sodium dodecyl sulfate (SDS), 69–70 Sodium hydroxide, 59 Soil carbon, 191–192 contamination, 57 excavation, 9 isolation, 38–39 liming, 186 microorganism, mining activity, impact of, 94, 95t mining activity, impact of, 94, 95t moisture, 186 organic matter, 384–385

pH, 383–384 pollution, gold mining, 379–380 replacement, 38 vitrification, 39 washing, 8, 40 Soil organic carbon (SOC), 325–326, 326f Solvent extraction, 75 South Africa fracking in, 473, 477–478 Mineral and Petroleum Resources Development Act (MPRDA), 479 National Development Plan (NDP), 479 shale gas development in, 477–482 water availability, 477 Spartina alterniflora, 276 Sphalerite, 89 Stabilization/solidification, 9 Strategic environmental assessment (SEA), 480 Strip mining, 170–171 Stylosanthes hamata, 349 Stylosanthes humilis, 348–349 Subsidence effects, 375 Sulfide metals, 379 Supercritical fluid extraction (SFE), 75–76 Superheated liquid extraction (SLE), 75–76 Superoxide dismutase (SOD), 12, 16 Surface Mining Control and Reclamation Act (SMCRA), 181, 188 Sustainability, 3 Switchgrass, 64–65 Synthetic precipitation leach procedure (SPLP), 177 Systemic biology approach, 494–495

T Tailing ponds, toxic elements in, 377 Technologically enhanced natural radiation (TENR), 250 Technosols, 330 Thallium, 497

514

Thermal power plant (TPP), 172–173, 175–176 Thiobacillus ferrooxidans, 378–379 Thlaspi caerulescens, 387, 389– 390, 397–398, 418–419 Total petroleum hydrocarbons (TPHs), 69–70, 458 Townsville lucerne. See Stylosanthes humilis Toxicants, phytoremediation of, 17–20 Toxicity, of heavy metals, 361, 361t animals, 8 plants, 7–8 Trace elements, 379 Transfer factor from soil (TFS), 493 Transgenic approaches, 494–495 in phytoremediation, 45–47, 46t Translocation factor (TF), 359–360 Transpiration, 385 Trifolium pratense L., 465 Tulsi. See Ocimum basilicum

U Ultrasound-assisted extraction (USAE), 75–76 Unavailable metals, 383 Underground mine, 374–375, 376f Uranium mine tailings characteristics, 251–252 in India, 250–251, 251f radionuclides accumulation, 257, 258t restoration techniques, 252–254 role of vegetation, 254, 254f, 255t selection of vegetation, 255–256

V Vachellia nilotica, 68–69 Vegetation, role of, 335–338, 337t Venezuela, 474–476 Vertical flow subsurface constructed wetlands (VSSFCW), 415–416 Vetiver grass, 69, 228 Vetiveria zizanioides, 350, 493 Viola calaminaria, 387

Index Viola tricolor, peroxidase activity, 364 Vitrification, 9

W Water contamination, 92–93, 93t Water effluents, 107

Water lettuce. See Pistia stratiotes Water pollution, gold mining, 378–379 West Virginia ash policy, 175

Z Zea mays-Streptomyces, 458

515

Zinc, 382 from gold ores, 382 hyperaccumulator, Noccaea caerulescens, 493 phytoremediation, 395–397t, 397–398 phytotoxicity, 386