Sustainable Cities and Society 46 (2019) 101381

Contents lists available at ScienceDirect

Sustainable Cities and Society

journal homepage: www.elsevier.com/locate/scs

Improving the quality of runoff from green roofs through synergistic biosorption and phytoremediation techniques: A review T ⁎ ⁎⁎ K. Vijayaraghavana,b, , D. Harikishore Kumar Reddyc, Yeoung-Sang Yunc, a Department of Chemical Engineering, Indian Institute of Technology Madras, Chennai 600036, India b Sino-Forest Applied Research Centre for Pearl River Delta Environment, Department of Biology, Hong Kong Baptist University, Hong Kong, PR China c Division of Semiconductor and Chemical Engineering, Chonbuk National University, Jeonbuk, 561-756, Republic of Korea

ARTICLE INFO ABSTRACT

Keywords: Urban rooftops covered with plants known as “green roofs” or “vegetative roofs” have recently attracted intense Green roofs research interest because of their unique benefits and recognition in various countries as a potential best Green buildings management practice. However, most of these benefits are just theoretical assumptions, and only few research Biosorption efforts have been performed to draw a definitive conclusion. Of these, the quality of runoff from vegetative roofs Phytoremediation often comes under debate. Hence, this critical review article primarily focuses on the quality of water from Stormwater quality vegetative roofs, as well as directions to achieve better quality runoff. This review briefly introduces the fun- Sustainable design damentals and benefits of vegetative roofs, followed by the quality of runoff as observed by other investigators. Until now, the vegetative roof substrate and plant types have not been selected based on their potential to decontaminate runoff. To improve the quality of runoff, we highlight the necessity to consider the sorption capacity of the substrate and phytoremediation potential of plants. For the first time, various sorbents that can be used as additives in the vegetative roof substrate, as well as practical plant species that can phytoextract con- taminants in the substrate are presented. Some recommendations regarding the future research are also pro- vided.

1. Introduction building (La Roche & Berardi, 2014; Ziogou, Michopoulos, Voulgari, & Zachariadis, 2018); (v) sound insulation and noise reduction (Connelly A vegetative roof implies planting vegetation on a building rooftop & Hodgson, 2015); (vi) improved air quality (Rowe, 2011); (vii) in- through defined engineering methods. It is a modern way of restoring creased aesthetic value of the building (Jungels, Rakow, Allred, & an ecosystem that was earlier destroyed by the rapid expansion of Skelly, 2013); (viii) protection of the roof membrane of the building building construction due to the migration of rural people to urban (Lata et al., 2018); and (ix) ecological preservation in cities (Johnston & centers (Satterthwaite, McGranahan, & Tacoli, 2010). Vegetative roofs Newton, 1995; Teotónio, Silva, & Cruz, 2018). Several developing and have several benefits, and are widely considered as a practical solution developed nations have recognized these unique advantages and started to make buildings more sustainable (Saadatian et al., 2013; Sangkakool, implementing, and in some instances mandating, the vegetative roofs in Techato, Zaman, & Brudermann, 2018; Wong, Tay, Wong, Ong, & Sia, urban structures. In 2015, France approved a new rule that mandates 2003), by providing a healthy environment with low energy con- all establishments that are newly created in commercial places to be sumption. Vegetative roofs offer numerous theoretical economic and partly installed with either vegetative roofs or photovoltaic panels. environmental benefits to the building underneath, as well as to the Other countries, such as Germany, Canada (Toronto), Denmark (Co- surrounding environment. Few of these benefits (Oberndorfer et al., penhagen), Japan (Tokyo) and Switzerland (Zürich), have already 2007; Rowe, 2011) include (i) runoff peak-flow reduction during high adopted mandatory vegetative roof by law. Vegetative roofs are also storm events (Morgan, Celik, & Retzlaff, 2013; Zhang, Szota, Fletcher, extremely popular in several European (Norway, Sweden and the UK), Williams, & Farrell, 2019); (ii) rainwater buffering (Vijayaraghavan, American (USA) and Asian (Singapore, China and Hong Kong) counties. Joshi, & Balasubramanian, 2012); (iii) mitigating urban heat island However, the importance and benefits of vegetative roofs are still not (Santamouris, 2014); (iv) decreased energy requirements of the recognized by several nations and their respective policy makers. This

⁎ Corresponding author at: Department of Chemical Engineering, Indian Institute of Technology Madras, Chennai, 600036, India. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (K. Vijayaraghavan), [email protected] (Y.-S. Yun). https://doi.org/10.1016/j.scs.2018.12.009 Received 23 September 2018; Received in revised form 4 December 2018; Accepted 7 December 2018 Available online 10 December 2018 2210-6707/ © 2018 Elsevier Ltd. All rights reserved. K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Table 1 Characteristics of different vegetative roof types.

Intensive vegetative roofs Extensive vegetative roofs

Thickness of substrate layer > 15 cm < 15 cm Weight Heavy; require concrete support Low; used with concrete, steel and/or timber support Type of plants Perennials, lawn, shrubs, small trees and rooftop farming Grass, herbs, mosses, sedums and other succulents Irrigation Constant irrigation using automated sprayer Required at fewer intervals Maintenance High Low Fertilizer application Required Not required Water proofing High-end Low-end Root-Barrier Required Not required Overall costs High Low might be due to the limited or lack of local research in the respective countries. Here we would like to give a brief introduction to vegetative roofs, including their characteristics and components, for the interest of readers new to this topic. Vegetative roofs are often regarded as eco- roofs, bio-roofs, and living-roofs, and are generally categorized into extensive and intensive vegetative roofs. Extensive vegetative roofs have a thin growth-substrate layer that can accommodate only a few species of plants, whereas intensive vegetative roofs comprise a thick growth-substrate layer and therefore support a wide variety of plant species. Table 1 summarizes important characteristics of different ve- getative roof types. We should point out that extensive vegetative roofs are the most common and popular worldwide. Some research reports have highlighted the possibility of achieving Fig. 1. Schematic of general vegetative roof system. potential benefits of vegetative roofs (Mahdiyar, Tabatabaee, Abdullah, & Marto, 2018; Morgan et al., 2013; Rowe, 2011). However, the focus for the appropriate selection of plants to improve the benefits, and to of commercial developers is often limited to the development of low- overcome difficult conditions prevailing on the rooftop, such as water weight growth substrate and its subsequent management (fertilization scarcity and extreme climatic conditions. On the other hand, substrate and irrigation) to facilitate plant growth (Berndtsson, 2010). As a result, is another essential component of the vegetative roof that directly in- most commercial vegetative roofing cannot accomplish all of the ben- fluences plant growth and also benefits vegetative roofs, including efits. This scenario is likely to change once more research reports stormwater runoff peak flow reduction and storage, rainwater buf- emerge, and also by close cooperation between academic researchers fering, energy savings, and sound insulation. Fig. 2 shows that typically and commercial developers. It is also important to understand the po- several inorganic and organic constituents are mixed at defined ratios tential constraint that hinders the positive image of a vegetative roof. to achieve a final vegetative roof substrate with the desired character- Of these, a crucial concern often linked with vegetative roof technology istics. The drainage layer plays a vital role in vegetative roofs, as it is the runoff quality, and several researchers have pointed out that the maintains a non-water-logged and aerated condition for the substrate to runoff quality from vegetative roofs is questionable, as it has been support healthy plant growth. Water stored between the pores of the found to contain several pollutants (Berndtsson, 2010; Vijayaraghavan, drainage material or in the compartments of drainage plastic modules 2016). It is known that plants and substrate components heavily in- can be utilized by plants during dry periods. The drainage element also fluence the runoff quality of vegetative roofs (Berndtsson, 2010). enhances the thermal properties of the vegetative roof and protects the However, research performed on these components to possibly improve waterproof membrane underneath (Saadatian et al., 2013). A filter the quality of runoff is relatively limited (Long, Clark, Berghage, & layer separates the substrate layer from the drainage element, thereby Baker, 2008; Vijayaraghavan & Joshi, 2015; Vijayaraghavan & Raja, preventing small components of growth substrate from obstructing the 2015a). Therefore, this review intends to systematically assess the drainage element. Several researchers have pointed out that the filter quality of runoff generated from vegetative roofs, and suggest ways to layer improves the total water absorption potential of vegetative roofs enhance the runoff quality. (Licht & Lundholm, 2006; Wong & Jim, 2014). Considering the wet nature of the vegetative roof, it is often advisable to utilize a water- proofing method. In the case of intensive vegetative roofs, a root-barrier 2. Components of vegetative roofs is essential; however it is not-mandatory for extensive type. The root- barrier serves as a guard of the roof deck to protect from the permeation The basic vegetative roof design comprises several components that of roots from hard plants. An insulation layer in the vegetative roof is include plants at the top, followed by growth substrate, filter compo- always optional, as it prevents the water retained in the vegetative roof nent, drainage element, and finally a water-proof membrane. Some from extracting heat in the winter or cooling the air in the summer. cases also include a protection layer, root barrier (intensive roofs), and Table 2 lists some of the most important vegetative roof components an insulation layer. Fig. 1 illustrates a schematic of the general vege- used in studies and their specifications. tative roof system. For the success of a vegetative roof, proper selection Of these essential components, both plants and substrate play cri- of these components and their combinations is very important tical roles in changing the quality of runoff from vegetative roofs. It (Vijayaraghavan, 2016). Fig. 2 lists basic selection criteria to design or should be noted several research studies have pointed out that vege- engineer vegetative roof components. Plants are the uppermost layer, tative roof runoff quality is a cause of concern (Berndtsson, 2010; and usually determine the visual success of the vegetative roof. Im- Vijayaraghavan, 2016). Considering that rainwater is relatively pure, provement of air quality, thermal performance, and heat-island issues apart from being acidic and containing traces of nutrients and metals, strongly depend on the type of plants grown on a vegetative roof (Cook- the magnitude of pollution caused by the vegetative roof is very high. It Patton & Bauerle, 2012). Thus, guidelines were recommended (Fig. 2)

2 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Fig. 2. Important vegetative roof components and their characteristics. is often reported that the vegetative roof produces runoff with high TDS vegetative roof only decreased the TSS concentrationas as well as (Beecham & Razzaghmanesh, 2015), TOC (Zhang et al., 2015), nu- neutralized the pH of rainwater. Alternatively, research performed on trients (Harper, Limmer, Showalter, & Burken, 2015), and metals vegetative roofs at the Augustenborg and Canoe Club House in Malmö, (Vijayaraghavan & Joshi, 2014b). While investigating a pilot-scale ve- Sweden showed that these roofs act as a source of heavy metals getative roof located on a structure in the Yubei district of Chongqing, (Berndtsson, Emilsson, & Bengtsson, 2006). Table 3 summarizes some China, Zhang et al. (2015) concluded that the vegetative roof increased important results regarding the quality of runoff water from vegetative 2+ − the concentrations of many components including BOD5,Ca ,Cl , roofs. In general, it can be concluded that the quality of runoff from − + + − 4+ 2− COD, DAl, DFe, DMn, DPb, F ,K ,NH4 -N, NO3 -N, Si ,SO4 , vegetative roofs is an important issue that must be addressed. Other- TN, and TOC. On a positive note, the authors indicated that the wise, this issue has the potential to negatively affect the positive

Table 2 Some important vegetative roof components used in the published literature.

Vegetative roof Type Details References component

Vegetation Sedum species Succulent; ground cover; drought tolerant; Moran, Hunt, & Jennings, 2003; Barker & used widely in extensive green roofs Lubell, 2012 Portulaca species Succulent; ground cover; used in extensive Vijayaraghavan & Joshi, 2015; Ye, Liu, roofs Zhao, Li, & Yu, 2013 Delosperma spices Succulent; ground cover; drought tolerant Hathaway, Hunt, & Jennings, 2008; Provenzano et al., 2010 Grasses More root growth; reduce water runoff; fast Nagase & Dunnett, 2012 growth and high biomass Growth substrate Vegetative roof substrate 20% vermiculite, 30% perlite; 20% crushed Vijayaraghavan & Raja, 2014b brick; 10% sand and 20% coco-peat Vegetative roof substrate 85% crushed brick, 5% compost, 5% Kuoppamäki et al., 2016 crushed bark and 5% sphagnum moss Commercial substrate Crushed lava, natural calcareous soil, clay, Berndtsson et al., 2006 and shredded peat Substrate mix Crushed brick, scoria, coir fibre, and Razzaghmanesh, Beecham, & Kazemi, composted organics 2014 Filter layer Geotextile fabric Decreases TSS Vijayaraghavan & Joshi, 2015 Geotextile material Prevents small particles from being washed Gong, Wu, Peng, Zhao, & Wang, 2014 from the substrate layer Drainage element Rubber crumbs Improved insulation and energy savings Pérez, Vila, Rincón, Solé, & Cabeza, 2012 LECA Cheap drainage element Karczmarczyk, Baryla, & Bus, 2014 Bioremegree drainage modules Costly; water storage capacity of 2 L/m2 Vijayaraghavan & Joshi, 2015 Floradrain FD40 Costly; water storage capacity of 4 L/m2 Hathaway et al., 2008 Lapillus Cheap option Gnecco, Palla, Lanza, & La Barbera, 2013 Norlite (coarse grade expanded shale) Cheap option Long et al., 2008 Water proofing Liquid-applied membranes, single ply sheet membranes, Protect roof, prevent leakage and act as root Townshend, 2007; Vijayaraghavan, 2016 modified-bitumen sheets and thermoplastic membranes barrier

3 .Vjyrgaa tal. et Vijayaraghavan K.

Table 3 Important results published on vegetative roof runoff quality.

Vegetative roof type Substrate Plants Country Runoff pollutants References

Pilot scale green roofs, extensive Potting mix Sedum mexicanum Singapore NO3 and PO4 Vijayaraghavan et al., 2012 Real green roof (8 years old), Commercial substrate (crushed lava, natural Sedum and moss Malmö, Sweden DOC, PO4 and K Berndtsson, Bengtsson, & Jinno, 2009 extensive calcareous soil, clay, and shredded peat) Pilot scale green roof, extensive Substrate mix (perlite, vermiculite, sand, crushed Portulaca grandiflora India TDS, Al, Fe, Cu, Ni, Zn, Vijayaraghavan & Joshi, 2014b brick and coco-peat) Pb and Cd Pilot scale green roofs, intensive Three substrate mixes (brick mix, Combination of Brachyscome multifida, Australia NO3,NO2,PO4,NH4,Na Beecham & Razzaghmanesh, 2015 and extensive scoria mix, Chrysocephalum apiculatum and Ca and organic mix) and Disphyma crassifolium

Real green roofs, extensive Light weight aggregates Several plant species such as Sedum, Gramineae and Estonia High pH, BOD7, TP and Teemusk & Mander, 2011 Thlaspi arvense PO4 Real green roof, extensive Substrate mix (crushed Wildflowers Toronto, Canada Ca, Mg and TP van Seters, Rocha, Smith, & volcanic rock, compost, peat, cooked clay, and MacMillan, 2009 sand)

4 Real green roof, extensive Commercial substrate 9 Sedum species Cincinnati, Ohio PO4 and DOC Buffam, Mitchell, & Durtsche, 2016 Pilot scale green roof, extensive Commercial substrate Seventeen species of Sedum and Phedimus takesimensis Missouri, USA TN and TP Harper et al., 2015 Pilot scale green roof, extensive Commercial substrate Sedum lineare Tianjin, China N and P Gong et al., 2014

Real green roof Substrate mix (lapillus, pumice, zeolite Grass Italy COD, TDS, Fe, Ca and K Gnecco et al., 2013 and peat) Pilot scale green roofs, extensive Several substrates (Arkalyte, Haydite and lava Sedum USA Pb, Cd and Cu Alsup, Ebbs, Battaglia, & Retzlaff, rock) with pine bark 2013 Pilot scale green roofs, extensive Substrate mix (42.5 % fine grade expanded shale, Sedum album, USA TP and color Long et al., 2008 42.5 % medium grade expanded Sedum spurium and Sedum sexangulare shale, 10% sphagnum peat moss, and 5% granulated activated carbon) Real green roof, extensive Substrate mix (15% compost and 85% inorganics) 9 Sedum species and 2 Delosperma species North Carolina, USA TN and TP Moran et al., 2003

Real green roof, extensive Commercial substrate (crushed lava, natural Sedum album, Malmö, Metals Berndtsson et al., 2006

calcareous soil, clay, and Sedum acre and other species Sweden Sustainable CitiesandS shredded peat) Real green roof 55% expanded slate, 30% Delosperma and Sedum species North Carolina, USA TN and TP Hathaway et al., 2008 sand and 15% composted cow manure Real green roof, intensive and Substrate mix (crushed brick, scoria, coir fibre Carpobrotus rossii, Lomandra longifolia Tanika, Dianella Adelaide, Australia High pH, turbidity, NO3, Razzaghmanesh et al., 2014 extensive and composted organics) caerula Breeze and Myoporum parvifofium PO4 and K ociety 46(2019)101381 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381 reputation of vegetative roofs. • High conductivity for hydraulics There are a variety of ways in which vegetative roofs can affect • Negligible organic components rainwater quality. For example, when rainwater percolates through the • Support for many different plant species vegetation and substrate, there is potential for both clean-up and con- • High efficiency to retain nutrients tamination. The vegetation may trap airborne particles and dust, thus • Ability to firmly anchor plants eliminating them from the rainwater. Also, the substrate material can • High stability act as an ion exchange filter for pollutants, nutrients, and trace metals present in rainwater. Overall, the vegetative roof components may act It is a complex undertaking to accomplish all the aforementioned as a sink if the ion concentration of the rainwater is high, and therefore characteristics via a single component, and thus a mixture of inorganic decreases the overall ion concentration in the final runoff. and organic components are often used in preparing the vegetative roof Alternatively, if the rainwater ion concentration is drastically lower substrate. In practice, substrates are made primarily of inorganic con- than that of the vegetative roof substrate, some ions will seep into the stituents with minimal organic content due to the fact that inorganic rainwater from the substrate. In effect, the runoff emanating from the constituents limit weed growth and eutrophic runoff conception. vegetative roof will have a higher ion concentration than the incoming Specifically, vegetative roof guidelines (DDC, 2007; FLL, rainwater. Other factors will also impact rainwater ion concentration, Forschungsgesellschaft Landschaftsentwicklung Landschaftsbau, 2002) such as fertilizers and soil microbes. The presence of fertilizer will recommend that inorganic constituents should comprise at least 80% of further complicate the leaching process, as it depends on plant uptake the substrate in order to lessen the weight of the system. Further, ac- and the mechanism of fertilizer release. The role of soil microbes is also cording to Forschungsgesellschaft Landschaftsentwicklung Land- imperative due to the fact that it directly modifies runoff quality. schaftsbau (FLL) guidelines, vegetative roof substrate should maintain a Hence, in summary, runoff quality from vegetative roofs is influenced wet bulk density ranging from 1000 to 1800 kg/m3, a dry bulk density by several facets, which are illustrated in Fig. 3. ranging from 600 to 1200 kg/m3, hydraulic conductivity greater than Analyzing all factors, we should point out that both the vegetative 3600 mm/h, greater than 10% AFP, and greater than 20% WHC (FLL, roof substrate and plants play critical roles in altering runoff quality. Forschungsgesellschaft Landschaftsentwicklung Landschaftsbau, 2002). Both of these factors can be controlled and manipulated to achieve the To achieve these limits, commercial developers often prepare vegeta- desired runoff quality. However, not many studies have focussed on tive roof substrate with high inorganic content, sometimes even devoid strategies to improve the quality of runoff. In the present review, we of organic constituents. These practices severely affect the growth of pay special attention to discuss the most vital components of vegetated plants. Vijayaraghavan et al. (2012) performed vegetative roof experi- roof: (i) plants, and (ii) substrate. ments with the commercial vegetative roof substrate (DAKU), and found that the substrate was unable to support the growth of vegetation 3. Substrate and sorption capacity (Sedum mexicanum) without fertilizer. Hence, adequate research should be directed to engineer an appropriate vegetative roof substrate that Substrate plays the role of synthetic soil in vegetative roofs, and is provides an essential environment for plant growth. essential for effective plant growth as well as overall success of vege- As stated above, lower limits of water holding capacity (WHC), bulk tative roofs. Considering that the growth substrate is the major portion density (ρb), high hydraulic conductivity (HC), and high air-filled por- of a vegetative roof, several characteristics or guidelines are required osity (AFP) are best for most commercial vegetative roof substrates. for substrate selection, including: Besides these, other factors such as plant support and good stability are not considered due to minimal or nil organic content in the substrate. • Minimal wet and dry bulk density Further, commercial substrate often requires fertilizer to support plant • High capacity to retain water growth which deteriorates the quality of runoff stemming from vege- • High porosity packed with air tative roofs. Gregoire and Clausen (2011) detected considerable amounts of both phosphorus and copper in the runoff from vegetative roofs primarily due to the presence of fertilizer. To improve the quality of runoff stemming from vegetative roofs, the sorption capacity of substrate materials should be considered as important selection criteria. Inorganic materials used in the vegetative roof substrate are often associated with less sorption capacity towards various pollutants. In such circumstances, to enhance the substrate’s overall sorption capability, organic components exhibiting high in- dividual sorption capacities are required in the vegetative roof sub- strate. Vijayaraghavan and Joshi (2014b) added coco-peat as the or- ganic fraction in vegetative roofs, and subsequently found that the vegetative roof system could retain 66.6 mg aluminum, 7.7 mg cad- mium, 15.1 mg chromium, 15.0 mg copper, 68.1 mg iron, 13.0 mg nickel, 8.8 mg lead, and 16.4 mg zinc from 70-mm metal-spiked pre- cipitation event. Vegetative roof substrate also contains many inorganic constituents including crushed brick, expanded clay, heat-expanded slate, perlite, pumice, recycled glass, sand, scoria, and vermiculite (Table 4). Most of these materials have nil to low sorption capacities towards various cations and anions. Kwon, Yun, Lee, Kim, and Jo, (2010) studied the use of scoria as an adsorbent to eliminate divalent metals such as cadmium, copper, lead, and zinc from the substrate. The results revealed that scoria possesses mediocre adsorption capacities of 1.48, 1.77, 2.41 and 6.93 mg/g for zinc, copper, cadmium, and lead, respectively. Similarly, Yavuz, Gode, Pehlivan, Ozmert, and Sharma, (2008) found that pumice fl ff Fig. 3. Factors that in uence runo quality in vegetative roofs. exhibited small adsorption capacities for copper and chromium of 3.5

5 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Table 4 The sorption capacity of some important inorganic constituents used in vegetative roof substrate.

Inorganic constituent Metals Adsorption capacity (mg/g) References

Scoria Pb 6.93 Kwon et al., 2010 Scoria Cu 1.77 Kwon et al., 2010 Scoria Zn 1.48 Kwon et al., 2010 Scoria Cd 2.41 Kwon et al., 2010 Scoria As(III) 1.59 Kwon et al., 2010 Scoria (Jeju, Korea) Zn 6.27 Kwon, Yun, Kim, Mayer, & Hutcheon, 2005

Sand NO3 5.85 Selvaraju & Pushpavanam, 2009 Sand Cl 2.19 Selvaraju & Pushpavanam, 2009

Sand PO4 3.33 Selvaraju & Pushpavanam, 2009 Sand Surfactant 2.16 Selvaraju & Pushpavanam, 2009 Sand Cu(II) 2.04 Wan, Petrisor, Lai, Kim, & Yen, 2004

Crushed brick NO3 14.1 Selvaraju & Pushpavanam, 2009 Crushed brick Cl 13.0 Selvaraju & Pushpavanam, 2009

Crushed brick PO4 18.2 Selvaraju & Pushpavanam, 2009 Crushed brick Surfactant 2.56 Selvaraju & Pushpavanam, 2009 Pumice Cu 3.5 Yavuz et al., 2008 Pumice Cr(III) 1.6 Yavuz et al., 2008 Perlite Pb 26.9 Vijayaraghavan & Raja, 2014a Perlite Cu 5.66 Vijayaraghavan & Raja, 2014a Perlite Cd 2.81 Vijayaraghavan & Raja, 2014a Perlite Ni 3.34 Vijayaraghavan & Raja, 2014a Vermiculite Pb 49.3 Vijayaraghavan & Raja, 2015b Vermiculite Cu 12.6 Vijayaraghavan & Raja, 2015b Vermiculite Cd 11.1 Vijayaraghavan & Raja, 2015b Vermiculite Ni 6.75 Vijayaraghavan & Raja, 2015b Vermiculite Pb 4.97 Abate & Masini, 2005 and 1.6 mg/g, respectively. On the other hand, perlite has shown good 3.1. Biosorbents sorption capacity for lead (26.9 mg/g), whereas poor sorption perfor- mance was shown for cadmium (2.81 mg/g), copper (5.66 mg/g), and Biosorption is an important bioremediation technique that makes nickel (3.34 mg/g) (Vijayaraghavan & Raja, 2014a). Table 4 sum- use of inactive or dead biological materials to sorb organic and in- marizes some important results on the adsorption performance of in- organic pollutants. Various physico-chemical mechanisms, such as ad- organic components towards various pollutants. By analyzing Table 4, sorption, ion-exchange, electrostatic interaction, complexation, co- we can generalize that the commonly used inorganic components ex- ordination, chelation, and microprecipitation are utilized to achieve hibited mediocre adsorption capacity toward most of the pollutants in pollutant removal (Vegliò & Beolchini, 1997; Vijayaraghavan & Yun, the substrate of the vegetative roof. This mediocre adsorption capacity 2008). In fact, several biosorbents were identified as possessing ex- should be compensated by adding high sorption capacity organic con- cellent sorption capacity, mainly originating from algae, fungi, bacteria, stituents to the substrate. It is also worth noting that because of their and agricultural and industrial wastes. Of these biosorbents, the se- chemical compositions, some of the inorganic materials deteriorate lected ones can be utilized as additives in vegetative roof substrate. runoff quality. For example, vermiculite, which is composed of oxides Considering that organic fractions in vegetative roofs are supplied to including SiO2,Al2O3,Fe2O3, and others (Vijayaraghavan & Raja, support plant growth, care should be taken to preserve the basic 2015b), can be expected to leach these elements over time into the properties of an organic fraction. Here, we would like to recommend runoff. several organic materials that can be used in the substrate, including (i) Organic constituents are essential in vegetative roof substrate, as seaweed, (ii) crab shell, and (iii) biochar. We subsequently provide they improve water retention potential, plant nutrients, stability to detailed individual discussions regarding their sorption performances. substrate, and anchorage to plants. Table 5 shows the organic fractions most commonly used in the vegetative roof substrate, which include coir, mulch, plant compost, bark, and peat. Further, organic compo- 3.1.1. Seaweeds nents usually possess better sorption capacity than their inorganic Seaweeds, also known as algae, are renewable natural biomasses, counterparts. For example, Jang, Seo, and Bishop, (2005) investigated which multiply rapidly and are plentiful throughout various ocean re- the adsorption capability of a variety of mulches including hardwood gions. Further, they have successfully been utilized as food for human bark, cypress bark, and pine bark nugget, and demonstrated good consumption (Fleurence, 2016), fertilizer (Craigie, 2011), and nour- sorption capacity values of 12.2 mg/g for zinc, 22.8 mg/g for copper, ishment for cattle (Bach, Wang, & McAllister, 2008). Seaweeds also and 72.5 mg/g for lead, when hardwood bark mulch was utilized in the supply important phycocolloids including alginic acid, agar, and car- substrate. Similarly, Parab et al. (2006) found that the coir pith main- rageenan (Rioux & Turgeon, 2015). Based on the biosorption capacity, tains decent adsorption capabilities toward chromium, cobalt, and seaweeds are found to be excellent biosorbents specifically for treating nickel of 11.6, 12.8, and 16.0 mg/g, respectively. It should be noted a variety of heavy metals (Davis, Volesky, & Mucci, 2003; Romera, that the vital organic components utilized in the substrate of vegetative González, Ballester, Blázquez, & Munoz, 2006). Algae can be classified roofs have average sorption capacities for common runoff pollutants, as by its cell wall chemistry, chlorophyllic nature, and flagellation. Ac- shown in Table 5. Considering that the fraction of the organic con- cordingly, they are divided into groups including Phaeophyta, Chlor- stituent is even less in the final substrate, it is desirable to use a material ophyta, Rhodophyta, Chrysophyta, Cryptophyta, Euglenophyta, Cya- with high sorption capacity without compromising other desirable nophyta and Charophyta (Davis et al., 2003). The first three divisions of properties. algae: Phaeophyta (brown algae), Rhodophyta (red algae), and Chlor- ophyta (green algae), are most common and commercially important. Typical cell walls of these three algae consist of a fibrillar skeleton which is most commonly composed of cellulose, but can be replaced by

6 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Table 5 The sorption capacity of some important organic constituents used in vegetative roof substrate.

Inorganic constituent Metals Adsorption capacity (mg/g) References

Coir pith Cr(VI) 165.0 Suksabye & Thiravetyan, 2012 Coir-pith Co 12.8 Parab et al. (2006) Coir-pith Cr 11.6 Parab et al. (2006) Coir-pith Ni 16.0 Parab et al. (2006) Peat Pb 47.8 Nwachukwu & Pulford, 2008 Peat Cu 11.8 Nwachukwu & Pulford, 2008 Peat Zn 4.2 Nwachukwu & Pulford, 2008 Mulch (Hardwood) Pb 72.5 Jang et al. (2005) Mulch (Hardwood) Cu 22.8 Jang et al. (2005) Mulch (Hardwood) Zn 12.2 Jang et al. (2005) Mulch (Madhuca longifolia) Pb 17.2 Rehman, Anwar, & Mahmud, 2013 Mulch (Polyalthia longifolia) Pb 4.50 Rehman et al., 2013 Green waste compost Pb 86.5 Nwachukwu & Pulford, 2008 Green waste compost Cu 30.2 Nwachukwu & Pulford, 2008 Green waste compost Zn 13.9 Nwachukwu & Pulford, 2008 Green waste compost Cu 30.2 Nwachukwu & Pulford, 2008 Wood bark Cu 17.1 Nwachukwu & Pulford, 2008 Wood bark Zn 11.0 Nwachukwu & Pulford, 2008 Bark compost Cu 4.7 Gichangi, Mnkeni, & Muchaonyerwa, 2012 Bark compost Pb 7.7 Gichangi et al., 2012 Bark compost Zn 2.6 Gichangi et al., 2012 Bark compost Ni 0.7 Gichangi et al., 2012

Table 6 The sorption capacity of recommended organic sorbents in vegetative roof substrate.

Sorbent Cation/Anion Sorption capacity (mg/g) References

Sargassum natans Cd 135.0 Holan, Volesky, & Prasetyo, 1993 Sargassum natans Pb 224.0 Jalali, Ghafourian, Asef, Davarpanah, & Sepehr, 2002 Sargassum fluitans Pb 330.0 Holan & Volesky, 1994 Ascophyllum nodosum Cu 58.8 Romera, González, Ballester, Blázquez, & Muñoz, 2007 Ascophyllum nodosum Cd 215.0 Holan et al., 1993 Ascophyllum nodosum Ni 43.3 Romera et al., 2007 Ascophyllum nodosum Pb 360.0 Holan & Volesky, 1994 Ascophyllum nodosum Zn 42.0 Romera et al., 2007 Ulva lactuca Pb 125.0 Jalali et al., 2002 Ulva sp. Mn 58.8 Vijayaraghavan & Joshi, 2014a Ulva sp. Cr(III) 150.3 Vijayaraghavan & Joshi, 2014a Ulva lactuca Cd 43.0 Bulgariu, Lupea, Bulgariu, Rusu, & Macoveanu, 2013 Kappaphycus alvarezii Cd 54.0 Praveen & Vijayaraghavan, 2015 Gracilaria corticata Pb 50.0 Jalali et al., 2002

Kappaphycus alvarezii PO4 59.8 Rathod et al., 2014 Kappaphycus alvarezii Ni 22.3 Praveen & Vijayaraghavan, 2015 Kappaphycus alvarezii Pb 105.7 Praveen & Vijayaraghavan, 2015 Crab shell (Chinonecetes opilio) Cd 199.0 An et al., 2001 Chinonecetes opilio Cr(III) 55.1 An et al., 2001 Ucides cordatus Cr(VI) 28.1 Niu & Volesky, 2003 Portunus trituberculatus Co 322.6 Vijayaraghavan et al., 2006b Portunus sanguinolentus Cu 243.9 Vijayaraghavan et al., 2006b P. trituberculatus Pb 870 Lee et al., 1998

Crab shell PO4 108.9 Jeon & Yeom, 2009 ○ Biochar (Thalia dealbata at 700 C) PO4 5.0 Zeng et al., 2013 ○ Biochar (Thalia dealbata at 700 C) NH4 17.6 Zeng et al., 2013 ○ Biochar (Canna indica at 500 C) Cd 188.8 Cui et al., 2016

Biochar (spent mushroom compost coated with Al(OH)3 )F 36.5 Chen et al., 2016 Biochar Cu 39.4 Liao, Cheng, Deng, & Xiao, 2016 Biochar Zn 57.8 Liao et al., 2016 Biochar Cd 26.7 Liao et al., 2016 Biochar Pb 28.9 Liao et al., 2016 xylan or mannan in the Chlorophyta, and only xylan in the Rhodophyta. biosorption capacities of 600, 478, and 330 mg/g, respectively. Table 6 Algae also consist of a shapeless embedding matrix which is pre- lists some important results that highlight the impressive biosorption dominantly composed of alginate or alginic acid with small amounts of performance of brown seaweeds towards various pollutants. Alginic sulfated polysaccharide (fucoidan) in the Phaeophyta. On the other acid, a linear carboxylated copolymer composed of varying proportions hand, the Rhodophyta is comprised of various sulfated galactans (Vo- of 1,4-linked β-D-mannuronic acid (M-block) and α-L-guluronic acid (G- lesky and Holan, 1995). Of these types, brown seaweeds performed block) (Haug, 1964), comprises approximately 10–40% of the dry exceedingly well in biosorption, owing to their chemical composition weight of brown algae (Davis et al., 2003). Specifically, the M- and G- (Davis et al., 2003; Romera et al., 2006). Holan and Volesky (1994) block sequences of alginic acid exhibit drastically different structures established that three species of brown algae, Fucus vesiculosus, Asco- and the proportion of these structures establish the reactivity and phyllum nodosum, and Sargassum fluitans, exhibited impressive Pb(II) physical properties of the polysaccharide (Romera et al., 2006).

7 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Alginate consists of carboxyl functional groups in abundance, in addi- 4.5. The maximum biosorption capacities were 150.3 mg Cr(III)/g and tion to hydroxyl groups and sulfonate groups of fucoidan. Each of these 58.8 mg Mn(II)/g as determined through the Langmuir model. In ad- chemical groups are critical in sorption efficiency depending on the ion dition, the authors determined that cell wall polysaccharides comprise type, ion charge, and environmental conditions such as the pH value approximately 38–54% or Ulva sp. on a dry weight basis and also because at lower values of pH, protonation of the functional groups contain a significant amount of ulvan, an anionic polyelectrolyte which with H + or other light metal ions suggests considerable occupancy of possesses a strong affinity towards metal cations due to the carboxylic the functional groups (Davis et al., 2003; Vijayaraghavan & Yun, 2008). and sulfate groups inside its structure. Additional details regarding Further raise in pH changes the overall surface charge of algae to ne- biosorption via green seaweeds can be found in Table 6. Green sea- gative due to a decrease in the concentration of H+ ions. This allows the weeds also showed good performance in continuous experiments algal surface to interact with cations. Several investigators highlighted (Apiratikul & Pavasant, 2008; Vijayaraghavan, Jegan, Palanivelu, & that biosorption was favourable in the pH range of 4–6 (mild-acidic to Velan, 2005), multi-component solutions (Areco, Hanela, Duran, & neutral pH condition) for cations. Considering that pH of rain water is Afonso, 2012; Plaza, Viera, Donati, & Guibal, 2011), and real waste- usually around this range, the algal biosorbent is expected to exhibit waters (Vijayaraghavan, 2008). Similarly, red seaweeds have been high biosorption capabilities. Further, binding of pollutants to seaweed shown to be efficient biosorption agents in column operation modes biosorbents is relatively strong, and hence strong acidic chemical so- (Vilar, Botelho, & Boaventura, 2008), batch operation modes (Rathod, lutions are required to desorb ions from bound seaweed biomasses Mody, & Basha, 2014), and metal-bearing wastewater treatment mod- (Vijayaraghavan & Yun, 2008). Kuyucak and Volesky (1989) utilized ules (Vilar, Martins, Botelho, & Boaventura, 2009). Considering the several desorbent solutions, including CaCl2, EDTA, HCl, H2SO4, KCl, extensive research undertaken to resolve the biosorption potential of KHCO3, KSCN, and NH4OH, to retrieve cobalt from Ascophyllum no- seaweeds over several decades, it is not difficult to suggest efficient and dosum loaded with the element. The sequestered cobalt could only be practical seaweeds as a biosorbent additive in vegetative roofs. eluted with greater than 96% desorption in a solution of 0.05 M CaCl2 There are many benefits that accompany addition of seaweed bio- in HCl at the optimal pH of 2-3. This information reveals that strong mass to vegetative roof substrates, primarily increased withholding of binding exists between the biomass and pollutants, and due to this, water due to seaweed swelling and absorption. Vijayaraghavan and metal ions are difficult to leach into the runoff. Further, the pollutant Raja (2015a) identified that Sargassum sp. had a water absorption ca- bound in the substrate will be taken from the system via the phytor- pacity of 260%, whereas Turbinaria conoides exhibited 170% water re- emediation ability of plants, and this topic will be covered in later parts tention capacity (Vijayaraghavan & Joshi, 2015). Syad, Shunmugiah, of the review. Brown seaweeds have also shown potential in con- and Kasi, (2013) reported the swelling water capacity of Sargassum tinuously purifying contaminated solutions (Davis et al., 2003; Volesky, wightii as 10 mL/g of dry weight. In biosorption applications, this Weber, & Park, 2003). Several investigators used packed column ar- property of seaweed is often considered as a drawback, as the swelling rangements to examine the possibility of brown seaweeds to con- phenomenon blocks the liquid flow and eventually increases the pres- tinuously biosorb pollutants (Park, Yun, & Park, 2010). Considering sure, which leads to stoppage of industrial wastewater treatment col- that the packed column closely resembles the vegetative roof arrange- umns. On the other hand, due to the presence of major inorganic ment, the results will be useful to discuss in the context of this review. components in vegetative roofs, the hydraulic conductivity is often very Through the use of a packed column, Volesky et al. (2003) demon- high. For example, crushed brick, which was widely used in vegetative strated that the biomass Sargassum filipendula sorption bed could be roof substrate, was reported to have a hydraulic conductivity of utilized for greater than 41 days of continuous operation to biosorb Cu 14,200 mm/h (Vijayaraghavan & Raja, 2014b). This severely affects the (II). On the other hand, Vijayaraghavan, Jegan, Palanivelu, and Velan, stormwater peak flow reduction potential of vegetative roofs. In such (2005) operated a Turbinaria ornata-loaded packed column for over 21 cases, constituents with high water retention and swelling potential days for the treatment of copper-bearing wastewaters. It is also well such as seaweeds can be useful to adjust excessive hydraulic con- known that contaminated waters in real situations often comprise ductivity. several metal ions, leading to competitive sorption in which one ion The seaweed family of plants are commonly utilized to augment contends against the others to get sorbed. Hence, it is vital to under- plant growth through their use as bio-fertilizers, bio-stimulants, and stand the performance of biosorbent under the presence of more than nutrient additives for soil. In common practice, vegetative roofs are one pollutant. With the aid of a hybrid Sargassum-sand loaded packed often supplied with chemical fertilizers (Berndtsson, 2010). These fer- column, Vijayaraghavan and Joshi (2013) treated ICP-OES wastewater tilizers result in contamination due to topsoil reduction (Denholm, under very low pH (pH – 1.1), high conductivity (6.98 mS/cm), and Devine, & Williamson, 2002) and toxic materials permeating into the TDS and salinity values of 4.46 g/L and 3.77, respectively. The waste- water runoff, thereby decreasing the overall quality of the vegetative water was comprised of 14 different metals including Al, Ca, Cd, Co, Cr, roof runo ff. Hence, it is advisable to utilize natural organic additives Cu, Fe, K, Mg, Mn, Na, Ni, Pb, and Zn. Notably, the authors observed such as seaweeds to promote plant growth and soil structure in vege- that many heavy metal ions were removed with high efficiency by the tative roofs. As previously noted, soil structure and plant growth can be Sargassum biosorbent. A few investigators also pointed out that the enhanced through the addition of seaweed which comprised of amino extreme conditions that prevail in real contaminated solutions also acids, metabolic enhancements, and both macro- and micro-nutrients hinder the performance of biosorbents. For example, extremely high or (Illera-Vives, Seoane Labandeira, Brito, López-Fabal, & López- low pH, high conductivity, high TDS, and high salinity were found to Mosquera, 2015). Further, seaweed is an ample source of potassium (K) affect the biosorption performance of seaweeds (Vijayaraghavan, and is also comprised of many growth activators including alginates, 2016). Vijayaraghavan, Palanivelu, and Velan, (2006) treated complex cytokines, and auxins (Illera-Vives et al., 2015). Important seaweeds electroplating wastewater (total hardness = 580 mg/L; TDS = 1489 utilized in commercial soil amendment include brown seaweeds, such mg/L; Ni content = 109 mg/L) using a Sargassum-loaded packed as Ascophyllum nodosum, Sargassum sp., Laminaria sp., Durvillaea sp. and column. The column effectively biosorbed Ni(II) ions with uptake ca- Ecklonia maxima. Several researchers highlighted the benefits of sea- pacity greater than 21.7 mg/g, and also showed potential to con- weed extracts as compost, such as enhanced growth and yield (Selvam tinuously treat wastewaters for five cycles. & Sivakumar, 2014), assistance in pest control of insects and soil ne- Green seaweeds are another division of algal biosorbents that per- matodes (Craigie, 2011), bio-stimulants cultivating plant tolerance to formed well in the removal of cations and anions (Hashim & Chu, 2004; abiotic and biotic stresses (Mercier et al., 2001), higher concentrations Murphy, Tofail, Hughes, & McLoughlin, 2009). Vijayaraghavan and of chlorophyll (Blunden, Jenkins, & Liu, 1997), timely seed germination Joshi (2014a) have demonstrated that the Ulva sp. biomass has a no- (Rathore et al., 2009), and retardance of senescence, thereby extending table biosorption capacity of the metals Cr(III) and Mn(II) at a pH of product shelf life.

8 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

3.1.2. Crab shell various environmental management issues, such as improvement of soil Crab shells have also been identified as a superior biosorbent for fertility (Kuoppamäki, Hagner, Lehvävirta, & Setälä, 2016), as an ad- various metals and other pollutants. The high sorption capacity is due sorbent (water and soil remediation) (Ding et al., 2016), and to mitigate to the presence of chitin and other proteins, in addition to calcium and environmental carbon (sequestration) (Rebitanim, Ghani, Rebitanim, & magnesium carbonates (An, Park, & Kim, 2001; Jeon & Yeom, 2009; Salleh, 2013). Hence, supplementation biochar in vegetative roof im- Lee, Park, & Yang, 1997). Seafood-based companies generate a huge proves the following properties of substrate: pH value (Jien & Wang, amount of solid waste, in particular, crab shell waste, and further uti- 2013), water-retention capability (Karhu, Mattila, Bergström, & Regina, lization or disposal of these wastes is still a major problem. Recycling 2011), nutrient retention (Clough, Condron, Kammann, & Müller, waste from crab shells would be greatly beneficial to the environment 2013), aeration (Cayuela et al., 2013), and hydraulic conductivity and possibly create additional earnings for the seafood industry. Recent (Buss, Kammann, & Koyro, 2012). Besides environmental aspects, usage reports estimate that crab shell waste totals millions of tons of per year, of biochar have additional benefits due to the fact that it can be pro- some specifically noting the annual disposal of 5000–8000 tons of these duced from low- or no-cost biomass feed stocks. Investigators also re- wastes from seafood industry (Niu & Volesky, 2003). Based on this, commended biochar in vegetative roofs, as it decreases the substrate several researchers looked at the utilization of crab shell wastes as weight (Cao, Farrell, Kristiansen, & Rayner, 2014), and improves runoff biosorbent (Lee et al., 1997), soil conditioner (Ali, Horiuchi, & quality (Beck, Johnson, & Spolek, 2011; Kuoppamäki et al., 2016). As a Miyagawa, 1998), plant fertilizer, (Adiloglu & Adiloglu, 2008) and vegetative roof substrate additive, biochar has specifically been found chitin preparation (Hajji, Ghorbel-Bellaaj, Younes, Jellouli, & Nasri, to have water retention capacities of 77% (Kuoppamäki et al., 2016) 2015). and 79.1% (Farrell, Cao, Ang, & Rayner, 2016). Beck et al. (2011) The presence of calcium carbonate is a primary factor responsible added 7% biochar in a vegetative roof substrate and observed im- for biosorbent properties of crab shells. Specifically, metal ions on the provement of runoff quality such as reduced runoff turbidity as well as surface of crab shells are micro-precipitated (Lee et al., 1997). In a pH- notable decreases in concentrations of total nitrogen, total phosphorus, dependent process, calcium carbonate dissociates into individual ions. nitrate, phosphorus, and organic carbon. Biochar acts as a slow-release When the individual calcium and carbonate ions contact metal ions, carrier for fertilizer (Jassal et al., 2015), increases the organic content metal carbonate precipitates are formed in the solution, and are sub- of the soil (Jha, Biswas, Lakaria, & Subba Rao, 2010), and increases the sequently adsorbed by the chitin present on the crab shell. Lee, Lee, soil microbe activity (Lehmann et al., 2011). Based on the aforemen- Shin, Kajiuchi, and Yang, (1998) removed Pb(II) from wastewater by tioned positive attributes, Githinji (2014) reported that the addition of employing raw crab shell particles and demonstrated that Pb became biochar positively enhanced the soil by decreasing the bulk density of 2− bound to –NHCOCH3 and CO3 through the dissolution of CaCO3, soil which led to an increased total soil porosity, thereby increasing soil which finally led to precipitation of Pb3(CO3)2(OH)2 and PbCO3.In aeration, water retention, and volumetric water content. As a result of addition, it has been shown that crab shells also have great sorption these positive attributes, the authors inferred that plant roots would capacities for toxic metals including lead (Lee et al., 1997), copper better be able to access sufficient oxygen and moisture resulting in (Vijayaraghavan, Palanivelu, & Velan, 2006), chromium (Kim, 2003), better plant growth. cobalt (Vijayaraghavan et al., 2006b), and arsenic (Niu, Volesky, & Biochar also demonstrated very good sorption capacity towards Cleiman, 2007). Crab shell was also efficient in the continuous re- various metal ions (Jiang, Jiang, Xu, & Li, 2012; Yakkala, Yu, Roh, mediation of metal ions in a packed column arrangement. Of these Yang, & Chang, 2013), anions (Wang et al., 2015; Zhang, Gao, Yao, packed column studies, Vijayaraghavan, Jegan, Palanivelu, and Velan, Xue, & Inyang, 2012), and organic pollutants (Ahmad, Moon et al., (2004) examined the removal of Ni(II) ions from aqueous solution via 2014, 2014b; Deng, Wang, Shi, & Hong, 2013). Yakkala et al. (2013) crab shell utilization. The authors observed that the crab shell-loaded prepared biochar from buffalo weed at different pyrolysis temperatures ○ column performed well over seven sorption-desorption cycles, with (300, 500 and 700 C). The results indicated that the biochar pyrolyzed ○ high Ni(II) biosorption capacity. It was also observed that crab shell at 700 C exhibited Cd(II) and Pb(II) sorption capacities of 11.6 and performed well to remediate multi-component solutions (Kim, 2003), as 333.3 mg/g, respectively. To successfully adsorb both cations and an- well as for real wastewaters (Vijayaraghavan, Palanivelu, & Velan, ions, biochar utilizes mechanisms such as ion exchange, surface com- 2005). plexation physical adsorption, electrostatic interactions, and pre- Crab shell can also be used as a soil amendment and an organic cipitation (Nartey & Zhao, 2014; Tan et al., 2015). Further, some of the fertilizer (Ali et al., 1998), and these features of crab shell can be ad- desirable physical properties of biochar include its micro-porosity and vantageous for plant growth due to the fact that the shell supplies es- high surface area (Ahmad, Moon et al., 2014, 2014b). As a result of sential nutrients (such as nitrogen and phosphorous) thus augmenting these properties, Reddy, Xie, and Dastgheibi, (2014) found that biochar the physical properties and organic content of the soil (Date, 1989). In effectively reduced TSS of the runoff by approximately 86%, the nitrate effect, these properties limit the need for costly inorganic fertilizers in concentration by 86%, and the phosphate concentration by 47%. In the vegetative roof substrate. Constituents of crab shell, namely chitin, addition, the concentrations of other metals were reduced between have the ability to control root pathogenic organisms biologically, 17–75%, with specific values as follows: cadmium, 18%; chromium, which can assist rhizobia reproduction and subsequently increase 19%; copper, 65%; lead, 75%; nickel, 17%; and zinc, 24%. symbiotic nitrogen fixation. Therefore, it is evident that crab shell is a Considering all of these factors, the development of a designated great organic component to be utilized for vegetative roof substrates. substrate for runoff water quality improvement from vegetative roofs, Adiloglu and Adiloglu (2008) observed that the available P phosphorus with a focus on nutrients and metals, is highly feasible. However, ad- content, pH value and exchangeable calcium and magnesium contents ditional efforts are needed to test the potential of these additives in real of acidic soils increased directly with the amount of crab shell powder case scenarios for extended periods. applied. Further, a study by Ali et al. (1998) determined that the crab shell amended soil enhanced soybean seed yield and growth at ma- 4. Vegetation and phytoremediation potential turity. The authors recommended that amending soil with crab shell could increase soybean seed yield to a similar level found when NPK Another key strategy to improve vegetative roof runoff quality is to fertilizer is used. select plants that have high phytoremediation ability. Plants with high phytoremediation ability could decrease the soil metal concentration 3.1.3. Biochar and thereby improve the runoff quality from vegetative roofs. Biochar is a solid carbon-rich product formed via pyrolysis under Phytoremediation is the direct utilization of plants and related micro- limited oxygen conditions. Biochar has been successfully employed in organisms found in soil to reduce the pollutant contamination of both

9 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Table 7 List of popular vegetative roof plants used for the remediation of heavy metals.

Plant species Metals Metal accumulation (mg/kg) References

Sedum alfredii Cd 4512 (stem); 3317 (leaf) Ni and Wei (2003) Portulaca oleracea Cr(VI) 4600 (roots); 1400 (stems) Alyazouria, Jewsburya, Tayimb, Humphreysa, & Al-Sayahb, 2013 Ficus microcarpa Cd 419 (overall) Yeo & Tan, 2011 Ficus microcarpa Cu 1260 (overall) Yeo & Tan, 2011 Ficus microcarpa Pb 1050 (overall) Yeo & Tan, 2011 Ficus microcarpa Zn 561 (overall) Yeo & Tan, 2011 Melastoma malabathricum Cd 426 (overall) Yeo & Tan, 2011 Melastoma malabathricum Cu 1820 (overall) Yeo & Tan, 2011 Melastoma malabathricum Pb 2390 (overall) Yeo & Tan, 2011 Melastoma malabathricum Zn 1380 (overall) Yeo & Tan, 2011 Pennisetum purpureum Cd 1.30 - 7.05 (shoot) Ishii, Hamano, Kang, Idota, & Nishiwaki, 2015 Helichrysum italicum Zn 646 (root); 1176 (shoot) Cao, Cappai, Carucci, & Muntoni, 2004 Helichrysum italicum Pb 346 (root); 484 (shoot) Cao et al., 2004 Portulaca grandiflora Pb 9.77 (overall) Cho-Ruk, Kurukote, Supprung, & Vetayasuporn, 2006 Sedum plumbizincicola Cd 35 (root); 93 (shoot) Ma et al., 2013 Sedum plumbizincicola Zn 889 (root); 1072 (shoot) Ma et al., 2013 Sedum plumbizincicola Pb 99 (root); 101 (shoot) Ma et al., 2013 Solanum nigrum Cd 35.9 (root); 77.0 (stem); 117.2 (leaf) Chen et al., 2014 Solanum nigrum Zn 167.9 (root); 95.4 (stem); 85.5 (leaf) Chen et al., 2014 Solanum nigrum Cu 64.0 (root); 12.3 (stem); 32.2 (leaf) Chen et al., 2014 Sedum alfredii Cd 923 (shoot); 137 (root) Wenhao, Hong, Mei, & Wuzhong, 2013 soil and water (Rajkumar, Sandhya, Prasad, & Freitas, 2012). This provide a remedy to pollutant contamination in soil via adsorption, technique is comprised of four independent plant-based methodologies, transport and translocation, hyperaccumulation or transformation, and namely: rhizofiltration, phytostabilization, phytovolatilization, and mineralization (Meagher, 2000), without suffering metal toxicity or cell phytoextraction. Rhizofiltration improves the quality of contaminated damage. These plants have an innate capability to accumulate heavy water by employing hydroponically grown plant roots to adsorb, con- metals in amounts of at least 100 times greater than those expected in centrate, and precipitate pollutants. On the other hand, phytostabil- average plants (Brooks, 1998). Tang et al. (2009) explored the metal ization uses plants to stabilize polluted soil and does not directly clean hyperaccumulation property of Arabis paniculata towards cadmium, or remove pollutants. Phytovolatilization is the consumption of pollu- lead, and zinc, and elucidated that the plant was hyper-tolerant to ex- tants by the plant, while phytoextraction is the consumption of pollu- cessive concentrations of these metals, accumulating average shoot tants by the plant roots and their subsequent transport to the aerial concentrations of 434 (Cd), 2300 (Pb), and 20,800 (Zn) mg/kg, while plant region. Of the different phytoremediation methods, plants with maintaining translocation factors above one. Literature also revealed high phytoextraction potential are most relevant to improve the nature that a popular vegetative roof plant, Sedum species hyperaccumulate of vegetative roof runoff. However, to date, no studies have been metals. In particular, Sedum alfredii, which grows in ancient lead-zinc published regarding the phytoremediation property as an important mining regions in Eastern China, was found to hyperaccumulate cad- factor in selecting plant species for vegetative roofs. Table 7 lists the mium (Sun, Ye, Wang, & Wong, 2007) and zinc (Lu et al., 2014); Long, phytoextraction potential of some of the popular vegetative roof plants Yang, Ye, Ni, and Shi, (2002) also reported the potential of Sedum al- used in several phytoremediation studies. freddi to hyperaccumulate zinc. Hence selecting vegetative roof plants It is often assumed that the metal-accumulation efficiency of parti- with high phytoextraction or hyperaccumulation properties is crucial to cular species of plants into its root cells is a crucial factor in the phy- the improvement of vegetative roof runoff quality. As reported by Yoon, toextraction process. However, it is actually essential that the sorbed Cao, Zhou, and Ma, (2006), hyperaccumulators are mostly character- metals be transported from the roots to the stem so that the accumu- ized as plant species with a translocation factor (TF) and a bioconcen- lated metals can be removed from the system (Tak, Ahmad, & Babalola, tration factor (BCF) greater than 1. 2013). This process is critical to achieve favorable and prolonged BCF implies the potential of metal accumulation in the plant roots benefits from a vegetative roof system, as there is a need to remove from the substrate, and can be represented (Yoon et al., 2006) as, metals from the system, which accumulate through the atmosphere, Croot through fertilizers, and through sorption by the substrate. Fig. 4 illus- BCF = C (1) trates possible mechanisms that may prevail during the phytoextraction substrate of metals from contaminated substrate in vegetative roofs. The move- where, Croot represents the concentration of metal present in the roots ment of metal ions from the root to stem is controlled by translocation, when harvested (mg/kg), and Csubstrate represents the metal con- a process which is comprised of leaf transpiration and root pressure centration initially measured in the substrate (mg/kg). (Lasat, 2002). Some metals are likely to accumulate in roots as a result The translocation factor (TF) describes the capacity of plants to of presumed physiological barriers which counter the transport of me- translocate metals to their shoots from the root region and can be tals to aboveground plant regions; while others can be mobilized shown (Yoon et al., 2006) as, without an issue. It should be noted that plants need some metals as Cshoot essential macro- and micro-nutrients for proper growth, including Ca, TF = C (2) Cu, Fe, K, Mg, Ni, and Zn. Despite the necessity for the aforementioned root metals, others including Al, Cd, Cr, and Pb, have not been observed to where, Cshoot is the concentration of metal present in the shoots when act physiologically. However, plants were identified to accumulate, or harvested (mg/kg). even hyperaccumulate, vital and dispensable metals through the phy- The phytoextraction property of plants strongly depends on the toextraction mechanism (Ghosh & Singh, 2005). Hyperaccumulator nature of metal species in the soil (Rajkumar et al., 2012). Metals are plants are a special category, consisting of approximately 400 species present in the substrate in a substate-controlled fluctuating equilibrium across 45 families (Saad-Allah & Elhaak, 2015). These plant types can as many different chemical species (Chaney, 1988). Of these, only a portion of these metals are bioavailable for plant intake (Lasat, 2002)as

10 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Fig. 4. Schematic for phytoextraction of metals from the contaminated substrate in vegetative roofs. most of the metals present are insoluble compounds that cannot be adapted in soil containing arsenic via the supplementation with five taken by plants (Sheoran, Sheoran, & Poonia, 2011). Further, the species of arsenate-reducing bacteria. The results were favourable, with phytoextraction capacity of plants can be limited by the continued arsenate-reducing bacteria encouraged P. vittata proliferation, in- presence of these metals in the soil making the bioavailability of metals creasing the build-up of arsenic, activating soil-insoluble arsenic, and in the soil a critical factor for the success of proper metal accumulation decreasing the leaching of arsenic as compared to the untreated control. by plants. Heavy metals and metalloids can be grouped into three Importantly, the biomass of Pteris vittata increased 53%, in part due to a subsets established via their soil bioavailability (Prasad, 2003): vastly 44% uptake of arsenic. In addition, contingent on the presence of ar- available (As, Cd, Cu, Ni, Se and Zn,); somewhat available (Co, Fe and senate-reducing bacteria, the leaching of arsenic was reduced by 29% Mn); and slightly available (Cr, Pb and U). To increase efficiency, plant (from 100% to 71%). In addition to studies of P. vittata, the metal ac- roots produce a material called phytosiderophore to aid in mobilizing cumulation properties of Sedum alfredii have also been investigated, metals in the rhizosphere (Lone, He, Stoffella, & Yang, 2008) which specifically through the utilization of the Burkholderia cepacia bac- assists in heavy metal solubilization (Ali, Khan, & Sajad, 2013). For terium by Li, Ye, and Wong, (2007). Here, the authors found that the instance, species of grass secrete siderophores (avenic and mugineic presence of Burkholderia cepacia significantly boosted S. alfredii pro- acids) which can increase sol iron bioavailability for uptake (Fushiya liferation (up to 110% with zinc treatment) and the uptake of metal by et al., 1982). In addition, root emission of H+ ions decreases the soil pH shoots (up to 243% and 96.3% with cadmium and zinc treatment, re- which consequently aids in rhizosphere acidification by dislodging spectively). The bacterium also aided better metal translocation from heavy metal cations from soil particles, thus encouraging metal dis- root to shoot (up to 296% and 135% with cadmium and zinc treatment, solution (Alford, Pilon-Smits, & Paschke, 2010). The decreased soil pH respectively) and increased the tolerance of S. alfredii to environmental increases the likelihood that metal ions will dislodge from soil particles, stresses (up to 134% with zinc added treatment). thus increasing the presence of heavy metals in the solution (Thangavel Considering all these advancements in phytoremediation tech- & Subbhuraam, 2004). However, taking into account that vegetative nology and its potential to remediate metal-contaminated soils, it is roof substrates are composed of an array of both organic and inorganic highly desirable to consider phytoremediation potential as an essential components along with the presence of several metal ions, it is difficult selection criterion for vegetative roof plants. Even some species of to identify effective vegetation that could remediate multiple metals. Sedum exhibited good phytoextraction, as well as hyperaccumulation To improve the phytoextraction performance of plants, several properties. Recently, to assess the quality of vegetative roof runoff, chemical additives, including limestone and chelating agents such as Vijayaraghavan and Joshi (2014b) compared vegetated and non-vege- EDTA, have been employed with positive results (Barrutia, Garbisu, tated roof constructions. The results suggested that vegetated (Portulaca Hernandez-Allica, Garcıa-Plazaola, & Becerril, 2010; Rajkumar et al., grandiflora) roof constructions yielded high quality runoff with low 2012). However, these chemicals are often phytotoxic as well as toxic to metal concentration, low conductivity, and low TDS. Similarly, beneficial soil microorganisms, and can leach into the final runoff. Beecham and Razzaghmanesh (2015) studied the runoff quality from Hence, research attention has focused on more environmentally benign vegetated (n = 12) and non-vegetated (n = 4) roofs over year. As an- techniques, which led to advancement of microbial-mediated techni- ticipated, concentrations of pollutants were greater in the runoff from ques in which microbial metabolites and processes in the rhizosphere non-vegetated systems as compared to vegetated systems. These limited change the bioavailability and movement capacity of metals, thus in- studies highlighted the possibility of runoff quality improvement fluencing the potential for metal uptake by plants (Glick, 2010; Ma, through plants; hence, more detailed research efforts are necessary to Rajkumar, Luo, & Freitas, 2013). Bacteria present in the soil can en- fully elucidate the phytoextraction potential of various plants to be courage root development, plant growth, and increase the resistance of utilized in vegetative roofs. plants to environmental stresses. Thus, bacteria utilization in soil to assist the process of metal phytoremediation has been a topic of interest 5. Conclusions for the past decade, and has proved successful in many instances (Glick, 2010). Table 8 lists some of the important vegetative roof plant species The vegetative roof is an efficient green strategy for managing that were examined in combination with bacteria for metal phytor- stormwater and improving energy savings, especially in space-limited emediation research studies. Yang, Tu, Wang, Liao, and Yan, (2012) urban cities. The other benefits of establishing vegetative roofs on attempted to enhance the arsenic uptake potential of Pteris vittata building tops are also well documented, and therefore several countries

11 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Table 8 Plant-bacteria combinations used in various metal phytoremediation research studies.

Plant species Associated bacteria Metals Effect of bacteria References

Sedum plumbizincicola Phyllobacterium myrsinacearum Cd, Zn and Improved metal accumulation; plant growth Ma et al., 2013 Pb Sedum plumbizincicola Bacillus pumilus E2S2 and Bacillus Cd and Zn Improved phytoextraction capacity; production of growth Ma et al., 2015 sp. E1S2 promoting/metal mobilizing metabolites/enzymes Solanum nigrum Pseudomonas sp. LK9 Cd, Zn and Production of biosurfactants; Chen et al., 2014 Cu siderophores; organic acids Sedum alfredii Pseudomonas veronii Zn Decreased soil pH; Long, Chen, Wong, Supplied P and Fe; better plant growth Wei, & Wu, 2013 Sedum alfredii Burkholderia sp. SaZR4, Burkholderia sp. Cd and Zn SaMR10 had little effect on phytoextraction; SaMR12 and SaNR1 Zhang et al., 2013 SaMR10, Sphingomonas sp. SaMR12 and promoted plant growth and phytoextraction of Zn and Cd; SaZR4 Variovorax sp. SaNR1 only promoted Zn-extraction

and municipalities have even started mandating vegetative roofs in new Alyazouria, A. H., Jewsburya, R. A., Tayimb, H. A., Humphreysa, P. N., & Al-Sayahb, M. buildings to make it more sustainable. Obviously, rapid research H. (2013). Phytoextraction of Cr(VI) from soil using Portulaca oleracea. Toxicological and Environmental Chemistry, 95, 1338–1347. growth in this area has recently stimulated a large amount of published An, H. K., Park, Y., & Kim, D. S. (2001). Crab shell for the removal of heavy metals from literature, and most of this literature highlights the benefits of vegeta- aqueous solution. Water Research, 35, 3551–3556. tive roofs. However, recently several drawbacks of vegetative roofs Apiratikul, R., & Pavasant, P. (2008). Batch and column studies of biosorption of heavy metals by Caulerpa lentillifera. Bioresource Technology Reports, 99, 2766 –2777 2008. have been put forward, which are overshadowing the positive status of Areco, M. M., Hanela, S., Duran, J., & Afonso, M. S. (2012). Biosorption of Cu(II), Zn(II), vegetative roofs. Of these, the most vital problem that must be ad- Cd(II) and Pb(II) by dead biomasses of green alga Ulva lactuca and the development of dressed is runoff quality. Several investigators reported vegetative roofs a sustainable matrix for adsorption implementation. Journal of Hazardous Materials, – – as a pollution source which impacts rainwater quality, but only few 213 214, 123 132. Bach, S. J., Wang, Y., & McAllister, T. A. (2008). Effect of feeding sun-dried seaweed research efforts have been devoted to tackle this problem. Through this (Ascophyllum nodosum) on fecal shedding of Escherichia coli O157:H7 by feedlot cattle review, we would like to recommend new strategies to choose substrate and on growth performance of lambs. Animal Feed Science and Technology, 142, – components and plant types to make the green roof sustainable. New 17 32. Barker, K. J., & Lubell, J. D. (2012). Effects of species proportions and fertility on sedum substrate materials and plants could replace the traditional and fre- green roof modules. HortTechnology, 22(2), 196–200. quently used counterparts. We suggest testing materials such as (i) Barrutia, O, Garbisu, C, Hernandez-Allica, J, Garcıa-Plazaola, JI, & Becerril, JM. (2010). seaweeds, (ii) crab shell, and (iii) biochar that has good water holding Differences in EDTA-assisted metal phytoextraction between metallicolous and non- ffi metallicolous accessions of Rumex acetosa L. Environmental Pollution, 158, capacity, high nutrient use e ciency, and high pollutant sorption ef- 1710–1715. ficiency to be employed as an additive in vegetated roof substrate. Beck, D. A., Johnson, G. R., & Spolek, G. A. (2011). Amending greenroof soil with biochar However, much research effort is required to test their soil compat- to affect runoff water quantity and quality. Environmental Pollution, 159, 2111–2118. fi Beecham, S., & Razzaghmanesh, M. (2015). Water quality and quantity investigation of ibility and their potential to achieve other bene ts of vegetative roofs. green roofs in a dry climate. Water Research, 70, 370–384. Cost is also a key factor, and thus researchers should pick low-cost Berndtsson, J. C. (2010). Green roof performance towards management of runoff water materials in substrates. Developing new and sustainable vegetative roof quantity and quality: A review. Ecological Engineering, 36, 351–360. Berndtsson, J. C., Emilsson, T., & Bengtsson, L. (2006). The influence of extensive ve- components will require extensive study supported by new experi- getated roofs on runoff water quality. The Science of the Total Environment, 355, mental techniques and strategies. 48–63. Berndtsson, J. C., Bengtsson, L., & Jinno, K. (2009). Runoff water quality from intensive – Acknowledgements and extensive vegetated roofs. Ecological Engineering, 35(3), 369 380. Blunden, G., Jenkins, T., & Liu, Y. (1997). Enhanced leaf chlorophyll levels in plants treated with seaweed extract. Journal of Applied Phycology, 8, 535–543. This work was supported by the Korean Government through NRF Brooks, R. R. (1998). Plants that hyperaccumulate heavy metals. Cambridge: CAB – (2014R1A2A1A09007378) grants. One of the authors (KV) was finan- International1 14. Buffam, I., Mitchell, M. E., & Durtsche, R. D. (2016). Environmental drivers of seasonal cially supported by a Ramalingaswami Re-entry Fellowship variation in green roof runoff water quality. Ecological Engineering, 91, 506–514. (Department of Biotechnology, Ministry of India, India), and by Brain- Bulgariu, L., Lupea, M., Bulgariu, D., Rusu, C., & Macoveanu, M. (2013). Equilibrium Korea 21 plus program. study of Pb(II) and Cd(II) biosorption from aqueous solution on marine green algae biomass. Environmental Engineering and Management Journal, 12, 183–190. Buss, W., Kammann, C., & Koyro, H.-W. (2012). Biochar reduces copper toxicity in References Chenopodium quinoawilld. in a sandy soil. Journal of Environmental Quality, 41, 1157. Cao, A., Cappai, G., Carucci, A., & Muntoni, A. (2004). Selection of plants for zinc and lead phytoremediation. Journal of Environmental Science and Health, 39(4), fl Abate, G., & Masini, J. C. (2005). In uence of pH, ionic strength and humic acid on 1011–1024. adsorption of Cd(II) and Pb(II) onto vermiculite. Colloids and Surfaces A, Cao, C. T. N., Farrell, C., Kristiansen, P. E., & Rayner, J. P. (2014). Biochar makes green – – Physicochemical and Engineering Aspects, 262(1 3), 33 39. roof substrates lighter and improves water supply to plants. Ecological Engineering, 71, Adiloglu, A., & Adiloglu, S. (2008). Amendment of acid soils using crab shell powder. 368–374. – Asian Journal of Chemistry, 20, 2156 2162. Cayuela, M. L., Sánchez-Monedero, M. A., Roig, A., Hanley, K., Enders, A., & Lehmann, J. Ahmad, M., Moon, D. H., Vithanage, M., Koutsospyros, A., Lee, S. S., Yang, J. E., et al. (2013). Biochar and denitrification in soils: when, how much and why does biochar (2014). Production and use of biochar from buffalo-weed (Ambrosia trifida L.) for reduce N2O emissions? Scientific Reports, 3, 1732. trichloroethylene removal from water. Journal of Chemical Technology & Chaney, R. L. (1988). Metal speciation and interactions among elements affect trace – Biotechnology, 89(1), 150 157. element transfer in agricultural and environmental food-chains. In J. R. Kramer, & H. Ahmad, M., Rajapaksha, A. U., Lim, J. E., Zhang, M., Bolan, N., Mohan, D., et al. (2014). E. Allen (Eds.). Metal speciation: Theory, analysis and applications (pp. 218–260). Biochar as a sorbent for contaminant management in soil and water: A review. Chelsea, MI: Lewis Publishers. – Chemosphere, 99,19 33. Chen, G. J., Peng, C. Y., Fang, J. Y., Dong, Y. Y., Zhu, X. H., & Cai, H. M. (2016). – Alford, E. R., Pilon-Smits, E. A. H., & Paschke, M. W. (2010). Metallophytes A view from Biosorption of fluoride from drinking water using spent mushroom compost biochar – the rhizosphere. Plant and Soil, 337,33 50. coated with aluminum hydroxide. Desalination and Water Treatment, 57(26), Ali, H., Khan, E., & Sajad, M. A. (2013). Phytoremediation of heavy metals-concepts and 12385–12395. – applications. Chemosphere, 91, 869 881. Chen, L., Luo, S., Li, X., Wan, Y., Chen, J., & Liu, C. (2014). Interaction of Cd-hyper- ff Ali, M., Horiuchi, T., & Miyagawa, S. (1998). E ects of soil amendment with crab shell on accumulator Solanum nigrum L. And functional endophyte Pseudomonas sp. Lk9 on the growth and nodulation of soybean plants (Glycine max Merr.). Plant Production soil heavy metals uptake. Soil Biology & Biochemistry, 68, 300–308. – Science, 1, 119 125. Cho-Ruk, K., Kurukote, J., Supprung, P., & Vetayasuporn, S. (2006). Perennial plants in ff Alsup, S., Ebbs, S., Battaglia, L., & Retzla , W. (2013). Green roof systems as sources or the phytoremediation of lead-contaminated soils. Biotechnology, 5,1–4. fl ff sinks in uencing heavy metal concentrations in runo . Journal of Environmental Clough, T., Condron, L., Kammann, C., & Müller, C. (2013). A review of biochar and soil Engineering, 139(4), 502–508.

12 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

nitrogen dynamics. Agronomy, 3, 275–293. adsorbent for the removal of high concentration of phosphate. Bioresource Technology Connelly, M., & Hodgson, M. (2015). Experimental investigation of the sound absorption Reports, 100, 2646–2649. characteristics of vegetated roofs. Building and Environment, 92, 335–346. Jha, P., Biswas, A. K., Lakaria, B. L., & Subba Rao, A. (2010). Biochar in agriculture - Cook-Patton, S. C., & Bauerle, T. L. (2012). Potential benefits of plant diversity on ve- prospects and related implications. Current Science, 99, 1218–1225. getated roofs: A literature review. Journal of Environmental Management, 106,85–92. Jiang, T.-Y., Jiang, J., Xu, R.-K., & Li, Z. (2012). Adsorption of Pb(II) on variable charge Craigie, J. S. (2011). Seaweed extract stimuli in plant science and agriculture. Journal of soils amended with rice-straw derived biochar. Chemosphere, 89(3), 249–256. Applied Phycology, 23, 371–393. Jien, S.-H., & Wang, C.-S. (2013). Effects of biochar on soil properties and erosion po- Cui, X., Fang, S., Yao, Y., Li, T., Ni, Q., Yang, X., et al. (2016). Potential mechanisms of tential in a highly weathered soil. CATENA, 110, 225–233. cadmium removal from aqueous solution by Canna indica derived biochar. The Science Johnston, J., & Newton, J. (1995). Building green: A guide to using plants on roofs, walls & of the Total Environment, 562, 517–525. pavements. London: London Ecology Unit. Date, N (1989). Soil amendment materials. In N. Date (Ed.). Hiryo binran (pp. 295–314). Jungels, J., Rakow, D. A., Allred, S. B., & Skelly, S. M. (2013). Attitudes and aesthetic Tokyo: Rural Culture Assoc. reactions toward green roofs in the Northeastern United States. Landscape and Urban Davis, T. A., Volesky, B., & Mucci, A. (2003). A review of the biochemistry of heavy metal Planning, 117,13–21. biosorption by brown algae. Water Research, 37, 4311–4330. Karczmarczyk, A., Baryla, A., & Bus, A. (2014). Effect of P-reactive drainage aggregates DDC (2007). DDC cool and green roofing manual. Prepared for New York City Department on green roof runoff quality. Water (Switzerland), 6(9), 2575–2589. of Design & Construction Office of Sustainable Design, by Gruzen Samton Architects Karhu, K., Mattila, T., Bergström, I., & Regina, K. (2011). Biochar addition to agricultural

LLP with Amis Inc., Flack & Kurtz Inc., Mathews Nielsen Landscape Architects P.C., soil increased CH4 uptake and water holding capacity – Results from a short-term and SHADE Consulting, LLC. pilot field study. Agriculture, Ecosystems & Environment, 140, 309–313. Deng, G., Wang, X., Shi, X., & Hong, Q. (2013). Adsorption characteristics of phenol in Kim, D. S. (2003). The removal by crab shell of mixed heavy metal ions in aqueous so- aqueous solution by Pinus massoniana biochar. Applied Mechanics and Materials, 295- lution. Bioresource Technology Reports, 87, 355–357. 298, 1154–1160. Kuoppamäki, K., Hagner, M., Lehvävirta, S., & Setälä, H. (2016). Biochar amendment in Denholm, I., Devine, G. J., & Williamson, M. S. (2002). Evolutionary genetics, insecticide the green roof substrate affects runoff quality and quantity. Ecological Engineering, resistance on the move. Science, 297, 2222–2223. 88,1–9. Ding, Y., Liu, Y., Liu, S., Li, Z., Tan, X., Huang, X., et al. (2016). Competitive removal of Kuyucak, N., & Volesky, B. (1989). Desorption of cobalt-laden algal biosorbent. Cd(II) and Pb(II) by biochars produced from water hyacinths: Performance and me- Biotechnology and Bioengineering, 33, 815–822. chanism. RSC Advances, 6, 5223–5232. Kwon, J.-S., Yun, S.-T., Lee, J.-H., Kim, S.-O., & Jo, H. Y. (2010). Removal of divalent Farrell, C., Cao, C. T. N., Ang, X. Q., & Rayner, J. P. (2016). Use of water-retention ad- heavy metals (Cd, Cu, Pb, and Zn) and arsenic(III) from aqueous solutions using ditives to improve performance of green roof substrates. Acta Horticulturae, 1108, scoria: Kinetics and equilibria of sorption. Journal of Hazardous Materials, 174, 271–278. 307–313 2010. Fleurence, J. (2016). Chapter 5 - seaweeds as food, in seaweed in health and disease pre- Kwon, J.-S., Yun, S.-T., Kim, S.-O., Mayer, B., & Hutcheon, I. (2005). Sorption of Zn(II) in vention. San Diego: Academic Press149–167. aqueous solutions by scoria. Chemosphere, 60, 1416–1426. FLL, Forschungsgesellschaft Landschaftsentwicklung Landschaftsbau (2002). Guideline for La Roche, P., & Berardi, U. (2014). Comfort and energy savings with active green roofs. the planning, execution and upkeep of green-roof sites. Forschungsgesellschaft Energy and Buildings, 82, 492–504. Landschaftsentwicklung Landschaftsbau e.V, Bonn. Lasat, M. M. (2002). Phytoextraction of toxic metals: A review of biological mechanisms. Fushiya, S., Takahashi, K., Nakatsuyama, S., Sato, Y., Nozoe, S., & Takagi, S. (1982). Co- Journal of Environmental Quality, 31, 109–120. occurrence of nicotianamine and avenic acids in Avena sativa and Oryza sativa. Lata, J. C., Dusza, Y., Abbadie, L., Barot, S., Carmignac, D., Gendreau, E., Kraepiel, Y., Phytochem, 21, 1907–1908. Mériguet, J., Motard, E., & Raynaud, X. (2018). Role of substrate properties in the Ghosh, M., & Singh, S. P. (2005). A review on phytoremediation of heavy metals and provision of multifunctional green roof ecosystem services. Applied Soil Ecology, 123, utilization of its byproducts. Applied Ecology and Environmental Research, 3,1–18. 464–468. Gichangi, E. M., Mnkeni, P. N. S., & Muchaonyerwa, P. (2012). Evaluation of the heavy Lee, M. Y., Lee, S. H., Shin, H. J., Kajiuchi, T., & Yang, J. W. (1998). Characteristics of lead metal immobilization potential of pine bark-based composts. Journal of Plant removal by crab shell particles. Process Biochemistry, 33, 749–753. Nutrition, 35(12), 1853–1865. Lee, M. Y., Park, J. M., & Yang, J. W. (1997). Micro precipitation of lead on the surface of Githinji, L. (2014). Effect of biochar application rate on soil physical and hydraulic crab shell particles. Process Biochemistry, 22, 671–677. properties of a sandy loam. Archives of Agronomy and Soil Science, 60(4), 457–470. Lehmann, J., Rillig, M. C., Thies, J., Masiello, C. A., Hockaday, W. C., & Crowley, D. Glick, B. R. (2010). Using soil bacteria to facilitate phytoremediation. Biotechnology (2011). Biochar effects on soil biota – a review. Soil Biology and Biochemistry, 43, Advances, 28, 367–374. 1812–1836. Gnecco, I., Palla, A., Lanza, L. G., & La Barbera, P. (2013). A green roof experimental site Li, W. C., Ye, Z. H., & Wong, M. H. (2007). Effects of bacteria on enhanced metal uptake of in the Mediterranean climate: The storm water quality issue. Water Science and the Cd/Zn-hyperaccumulating plant, Sedum alfredii. Journal of Experimental Botany, Technology: A Journal of the International Association on Water Pollution Research, 58, 4173–4182. 68(6), 1419–1424. Liao, Y., Cheng, Q., Deng, F., & Xiao, B. (2016). Adsorption of heavy metals in swine Gong, K., Wu, Q., Peng, S., Zhao, X., & Wang, X. (2014). Research on the characteristics of wastewater using bio-char. Chinese Journal of Environmental Engineering, 10(4), the water quality of rainwater runoff from green roofs. Water Science and Technology: 1842–1846. A Journal of the International Association on Water Pollution Research, 70, 1205–1210. Licht, J., & Lundholm, J. (2006). Native coastal plants for north eastern extensive and semi- Gregoire, B. G., & Clausen, J. C. (2011). Effect of a modular extensive green roof on intensive greenroof trays: Substrates, fabrics and plant selection. Paper Presented at the The stormwater runoff and water quality. Ecological Engineering, 37(6), 963–969. Fourth Annual Greening Rooftops for Sustainable Communities Conference. Hajji, S., Ghorbel-Bellaaj, O., Younes, I., Jellouli, K., & Nasri, M. (2015). Chitin extraction Lone, M. I., He, Z., Stoffella, P. J., & Yang, X. (2008). Phytoremediation of heavy metal from crab shells by Bacillus bacteria. Biological activities of fermented crab super- polluted soils and water: Progresses and perspectives. Journal of Zhejiang University natants. International Journal of Biological Macromolecules, 79, 167–173. Science B, 9, 210–220. Harper, G. E., Limmer, M. A., Showalter, W. E., & Burken, J. G. (2015). Nine-month Long, B. V., Clark, S. E., Berghage, R., & Baker, K. (2008). Green roofs - A BMP for urban evaluation of runoff quality and quantity from an experiential green roof in Missouri. stormwater quality? World Environmental and Water Resources Congress, 1–11. https:// USA. Ecol. Eng. 78, 127–133. doi.org/10.1061/40976(316)37. Hashim, M. A., & Chu, K. H. (2004). Biosorption of cadmium by brown, green and red Long, X.-X., Chen, X.-m., Wong, J. W.-C., Wei, Z.-B., & Wu, Q.-T. (2013). Feasibility of seaweeds. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 97, 249–255. enhanced phytoextraction of Zn contaminated soil with Zn mobilizing and plant Hathaway, A. M., Hunt, W. F., & Jennings, G. D. (2008). A field study of green roof growth promoting endophytic bacteria. Transactions of Nonferrous Metals Society of hydrologic and water quality performance. Transactions of the ASABE, 51(1), 37–44. China, 23(8), 2389–2396. Haug, A (1964). Composition and properties of alginates. Trondheim, Norway: Rept. 30. Long, X. X., Yang, X. E., Ye, Z. Q., Ni, W. Z., & Shi, W. Y. (2002). Differences of uptake and Norwegian Inst. of Seaweed Res123. accumulation of zinc in four species of Sedum. Acta Botanica Sinica, 44, 152–157. Holan, Z. R., & Volesky, B. (1994). Biosorption of lead and nickel by biomass of marine Lu, L., Liao, X., Labavitch, J., Yang, X., Nelson, E., Du, Y., et al. (2014). Speciation and algae. Biotechnology and Bioengineering, 43, 1001–1009. localization of Zn in the hyperaccumulator Sedum alfredii by extended X-ray ab- Holan, Z. R., Volesky, B., & Prasetyo, I. (1993). Biosorption of cadmium by biomass of sorption fine structure and micro-X-ray fluorescence. Plant Physiology and marine algae. Biotechnology and Bioengineering, 41, 819–825. Biochemistry, 84, 224–232. Illera-Vives, M., Seoane Labandeira, S., Brito, L. M., López-Fabal, A., & López-Mosquera, Ma, Y., Oliveira, R. S., Nai, F., Rajkumar, M., Luo, Y., Rocha, I., et al. (2015). The hy- M. E. (2015). Evaluation of compost from seaweed and fish waste as a fertilizer for peraccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria horticultural use. Scientia Horticulturae, 186, 101–107. that improve its phytoextraction capacity in multi-metal contaminated soil. Journal of Ishii, Y., Hamano, K., Kang, D.-J., Idota, S., & Nishiwaki, A. (2015). Cadmium phytor- Environmental Management, 156,62–69. emediation potential of Napiergrass cultivated in Kyushu, Japan. Applied and Ma, Y., Rajkumar, M., Luo, Y., & Freitas, H. (2013). Phytoextraction of heavy metal Environmental Soil Science, 2015, 6 Article ID 756270. polluted soils using Sedum plumbizincicola inoculated with metal mobilizing Jalali, R., Ghafourian, H., Asef, Y., Davarpanah, S. J., & Sepehr, S. (2002). Removal and Phyllobacterium myrsinacearum RC6b. Chemosphere, 93, 1386–1392. recovery of lead using nonliving biomass of marine algae. Journal of Hazardous Mahdiyar, A., Tabatabaee, S., Abdullah, A., & Marto, A. (2018). Identifying and assessing Materials, 92, 253–262. the critical criteria affecting decision-making for green roof type selection. Sustainable Jang, A., Seo, Y., & Bishop, P. L. (2005). The removal of heavy metals in urban runoff by Cities and Society, 39, 772–783. sorption on mulch. Environmental Pollution, 133, 117–127. Meagher, R. B. (2000). Phytoremediation of toxic elemental and organic pollutants. Jassal, R. S., Johnson, M. S., Molodovskaya, M., Black, T. A., Jollymore, A., & Sveinson, K. Current Opinion in Plant Biology, 3(2), 153–162. (2015). Nitrogen enrichment potential of biochar in relation to pyrolysis temperature Mercier, L., Lafitte, C., Borderies, G., Briand, X., Esquerré-Tugayé, M. T., & Fournier, J. and feedstock quality. Journal of Environmental Management, 152, 140–144. (2001). The algal polysaccharide carrageenans can act as an elicitor of plant defense. Jeon, D. J., & Yeom, S. H. (2009). Recycling wasted biomaterial, crab shells, as an The New Phytologist, 149,43–51.

13 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Moran, A., Hunt, B., & Jennings, G. A. (2003). North Carolina field study to evaluate 001. green roof runoff quantity, runoff quality, and plant growth. ASCE Conf. Proc. 118, Saadatian, O., Sopian, K., Salleh, E., Lim, C. H., Riffat, S., Saadatian, E., et al. (2013). A 335. https://doi.org/10.1061/40685(2003)335. review of energy aspects of green roofs. Renewable and Sustainable Energy Reviews, 23, Morgan, S., Celik, S., & Retzlaff, W. (2013). Green roof storm-water runoff quantity and 155–168. quality. Journal of Environmental Engineering (New York, NY), 139, 471–478. Sangkakool, T., Techato, K., Zaman, R., & Brudermann, T. (2018). Prospects of green Murphy, V., Tofail, S. A. M., Hughes, H., & McLoughlin, P. (2009). A novel study of roofs in urban Thailand – A multi-criteria decision analysis. Journal of Cleaner hexavalent chromium detoxification by selected seaweed species using SEM-EDX and Production. https://doi.org/10.1016/j.jclepro.2018.06.060 In Press. XPS analysis. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 148, Santamouris, M. (2014). Cooling the cities – A review of reflective and green roof miti- 425–433. gation technologies to fight heat island and improve comfort in urban environments. Nagase, A., & Dunnett, N. (2012). Amount of water runoff from different vegetation types Solar Energy, 103, 682–703. on extensive green roofs: Effects of plant species, diversity and plant structure. Satterthwaite, D., McGranahan, G., & Tacoli, C. (2010). Urbanization and its implications Landscape Urban Plan. 104(3-4), 356–363. for food and farming. Philosophical Transactions of the Royal Society of London Series B, Nartey, O. D., & Zhao, B. (2014). Biochar preparation, characterization, and adsorptive Biological Sciences, 365(1554), 2809–2820. capacity and its effect on bioavailability of contaminants: An overview. Advances in Selvam, G. G., & Sivakumar, K. (2014). Influence of seaweed extract as an organic fer- Materials Science and Engineering, 12 Article ID 715398. tilizer on the growth and yield of Arachis hypogea L. and their elemental composition Ni, T. H., & Wei, Y. Z. (2003). Subcellular distribution of cadmium in mining ecotype using SEM–Energy Dispersive Spectroscopic analysis. Asian Pacific Journal of Sedum alfredii. Acta Botanica Sinica, 45, 925–928. Reproduction, 3,18–22. Niu, H., & Volesky, B. (2003). Characteristics of anionic metal species biosorption with Selvaraju, N., & Pushpavanam, S. (2009). Adsorption characteristics on sand and brick waste crab shells. Hydrometallurgy, 71, 209–215. beds. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 147, 130–138. Niu, C. H., Volesky, B., & Cleiman, D. (2007). Biosorption of arsenic(V) with acid-washed Sheoran, V., Sheoran, A., & Poonia, P. (2011). Role of hyperaccumulators in phytoex- crab shells. Water Research, 41, 2473–2478. traction of metals from contaminated mining sites: A review. Critical Reviews in Nwachukwu, O. I., & Pulford, I. D. (2008). Comparative effectiveness of selected ad- Environmental Science and Technology, 41, 168–214. sorbant materials as potential amendments for the remediation of lead-, copper- and Suksabye, P., & Thiravetyan, P. (2012). Cr(VI) adsorption from electroplating plating zinc-contaminated soil. Soil Use Management, 24(2), 199–207. wastewater by chemically modified coir pith. Journal of Environmental Management, Oberndorfer, E., Lundholm, J., Bass, B., Coffman, R. R., Doshi, H., Dunnett, N., et al. 102,1–8. (2007). Green roofs as urban ecosystems: Ecological structures, functions, and ser- Sun, Q., Ye, Z. H., Wang, X. R., & Wong, M. H. (2007). Cadmium hyperaccumulation leads vices. Biosciences, 57, 823–833. to an increase of glutathione rather than phytochelatins in the cadmium hyper- Parab, H., Joshi, S., Shenoy, N., Lali, A., Sarma, U. S., & Sudersanan, M. (2006). accumulator Sedum alfredii. Journal of Plant Physiology, 164, 1489–1498. Determination of kinetic and equilibrium parameters of the batch adsorption of Co Syad, A. N., Shunmugiah, K. P., & Kasi, P. D. (2013). Seaweeds as nutritional supple- (II), Cr(III) and Ni(II) onto coir pith. Process Biochemistry, 41, 609–615. ments: Analysis of nutritional profile, physicochemical properties and proximate Park, D., Yun, Y.-S., & Park, J. M. (2010). The past, present, and future trends of bio- composition of G. Acerosa and S. Wightii. Biomedicine & Preventive Nutrition, 3, sorption. Biotechnology and Bioprocess Engineering : BBE, 15,86–102. 139–144. Pérez, G., Vila, A., Rincón, L., Solé, C., & Cabeza, L. F. (2012). Use of rubber crumbs as Tak, H. I., Ahmad, F., & Babalola, O. O. (2013). Advances in the application of plant drainage layer in green roofs as potential energy improvement material. ACS Applied growth-promoting rhizobacteria in phytoremediation of heavy metals. Reviews of Energy Materials, 97, 347–354. Environmental Contamination and Toxicology, 223,33–52. Plaza, J., Viera, M., Donati, E., & Guibal, E. (2011). Biosorption of mercury by Macrocystis Tan, X., Liu, Y., Zeng, G., Wang, X., Hu, X., Gu, Y., et al. (2015). Application of biochar for pyrifera and Undaria pinnatifida:Influence of zinc, cadmium and nickel. Journal of the removal of pollutants from aqueous solutions. Chemosphere, 125,70–85. Environmental Sciences (China), 23, 1778–1786. Tang, Y.-T., Qiu, R.-L., Zeng, X.-W., Ying, R.-R., Yu, F.-M., & Zhou, X.-Y. (2009). Lead, Prasad, M. N. V. (2003). Phytoremediation of metal-polluted ecosystems: Hype for zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata commercialization. Russian Journal of Plant Physiology: A Comprehensive Russian Franch. Environ. Experimental Botany, 66, 126–134. Journal on Modern Phytophysiology, 50, 686–700. Teemusk, A., & Mander, Ü. (2011). The influence of green roofs on runoff water quality: A Praveen, R. S., & Vijayaraghavan, K. (2015). Optimization of Cu(II), Ni(II), Cd(II) and Pb case study from Estonia. Water Resources Management, 25(14), 3699–3713. (II) biosorption by red marine alga Kappaphycus alvarezii. Desalination and Water Teotónio, I., Silva, C. M., & Cruz, C. O. (2018). Eco-solutions for urban environments Treatment, 55, 1816–1824. regeneration: The economic value of green roofs. Journal of Cleaner Production, 199, Provenzano, M. E., Cardarelli, M., Saccardo, F., Colla, G., Battistelli, A., & Proietti, S. 121–135. (2010). Evaluation of perennial herbaceous species for their potential use in a green roof Thangavel, P., & Subbhuraam, C. (2004). Phytoextraction: Role of hyperaccumulators in under mediterranean climate conditions. ISHS Acta Horticulturae 881: II International metal contaminated soils. Proceedings of the Indian National Science Academy Part B, Conference on Landscape and Urban Horticulture661–667. 70, 109–130. Rajkumar, M., Sandhya, S., Prasad, M. N. V., & Freitas, H. (2012). Perspectives of plant- Townshend, D. (2007). Study on green roof application in Hong Kong. Final Report, associated microbes in heavy metal phytoremediation. Biotechnology Advances, 30, 42–53. 1562–1574. van Seters, T., Rocha, L., Smith, D., & MacMillan, G. (2009). Evaluation of green roofs for Rathod, M., Mody, K., & Basha, S. (2014). Efficient removal of phosphate from aqueous runoff retention, runoff quality, and leachability. Water Quality Research Journal of solutions by red seaweed, Kappaphycus alverezii. Journal of Cleaner Production, 84, Canada, 44(1), 33–47. 484–493. Vegliò, F., & Beolchini, F. (1997). Removal of metals by biosorption: A review. Rathore, S. S., Chaudhary, D. R., Boricha, G. N., Ghosh, A., Bhatt, B. P., Zodape, S. T., Hydrometallurgy, 44, 301–316. et al. (2009). Effect of seaweed extract on the growth, yield and nutrient uptake of Vijayaraghavan, K. (2008). Biosorption of nickel from synthetic and electroplating in- soybean (Glycine max) under rainfed conditions. South African Journal of Botany : dustrial solutions using a green marine algae Ulva reticulata. Clean : Soil, Air, Water, Official Journal of the South African Association of Botanists = Suid-Afrikaanse Tydskrif 36, 299–305. Vir Plantkunde : Amptelike Tydskrif Van Die Suid-Afrikaanse Genootskap Van Vijayaraghavan, K. (2016). Green roofs: A critical review on the role of components, Plantkundiges, 75, 351–355. benefits, limitations and trends. Renewable & Sustainable Energy Reviews, 57, 740–752. Razzaghmanesh, M., Beecham, S., & Kazemi, F. (2014). Impact of green roofs on storm- Vijayaraghavan, K., & Joshi, U. M. (2013). Hybrid Sargassum-sand sorbent: A novel ad- water quality in a South Australian urban environment. The Science of the Total sorbent in packed column to treat metal-bearing wastewaters from inductively cou- Environment, 470-471, 651–659. pled plasma-optical emission spectrometry. Journal of Environmental Science and Rebitanim, N. Z., Ghani, W. A. W. A. K., Rebitanim, N. A., & Salleh, M. A. M. (2013). Health, Part A, 48, 1685–1693. Potential applications of wastes from energy generation particularly biochar in Vijayaraghavan, K., & Joshi, U. M. (2015). Application of seaweed as substrate additive in Malaysia. Renewable and Sustainable Energy Reviews, 21, 694–702. green roofs: Enhancement of water retention and sorption capacity. Landscape Urban Reddy, K. R., Xie, T., & Dastgheibi, S. (2014). Evaluation of biochar as a potential filter Plan. 143,25–32. media for the removal of mixed contaminants from urban storm water runoff. Journal Vijayaraghavan, K., & Joshi, U. (2014a). Application of Ulva sp. Biomass for single and of Environmental Engineering (New York, NY), 140 04014043. binary biosorption of chromium(III) and manganese(II) ions: Equilibrium modeling. Rehman, R., Anwar, J., & Mahmud, T. (2013). Sorptive removal of lead (II) from water Environmental Progress & Sustainable Energy, 33, 147–153. using chemically modified mulch of Madhuca longifolia and Polyalthia longifolia as Vijayaraghavan, K., & Joshi, U. (2014b). Can green roof act as a sink for contaminants? A novel biosorbents. Desalination and Water Treatment, 51, 2624–2634. methodological study to evaluate runoff quality from green roofs. Environmental Rioux, L.-E., & Turgeon, S. L. (2015). In B. K. Tiwari, & D. J. Troy (Eds.). Chapter 7 - Pollution, 194, 121–129. seaweed carbohydrates, in seaweed sustainability (pp. 141–192). San Diego: Academic Vijayaraghavan, K., & Raja, F. D. (2014a). Experimental characterisation and evaluation Press. of perlite as a sorbent for heavy metal ions in single and quaternary solutions. Journal Romera, E., González, F., Ballester, A., Blázquez, M. L., & Munoz, J. A. (2006). of Water Process Engineering, 4, 179–184. Biosorption with algae: A statistical review. Critical Reviews in Biotechnology, 26, Vijayaraghavan, K., & Raja, F. D. (2015a). Pilot-scale evaluation of green roofs with 223–235. Sargassum biomass as an additive to improve runoff quality. Ecological Engineering, 75, Romera, E., González, F., Ballester, A., Blázquez, M. L., & Muñoz, J. A. (2007). 70–78. Comparative study of biosorption of heavy metals using different types of algae. Vijayaraghavan, K., & Raja, F. D. (2014b). Design and development of green roof sub- Bioresource Technology Reports, 98, 3344–3353. strate to improve runoff water quality: Plant growth experiments and adsorption. Rowe, D. B. (2011). Green roofs as a means of pollution abatement. Environmental Water Research, 63,94–101. Pollution, 159, 2100–2110. Vijayaraghavan, K., & Raja, F. D. (2015b). Interaction of vermiculite with Pb(II), Cd(II), Saad-Allah, K. M., & Elhaak, M. A. (2015). Hyperaccumulation activity and metabolic Cu(II) and Ni(II) ions in single and quaternary mixtures. Clean : Soil, Air, Water, 43(8), responses of Solanum nigrum in two differentially polluted growth habitats. Journal 1174–1180. of the Saudi Society of Agricultural Sciences. https://doi.org/10.1016/j.jssas.2015.08. Vijayaraghavan, K., & Yun, Y.-S. (2008). Bacterial biosorbents and biosorption.

14 K. Vijayaraghavan et al. Sustainable Cities and Society 46 (2019) 101381

Biotechnology Advances, 26, 266–291. (Ambrosia trifida L. Var. trifida) biochar for cadmium (II) and lead (II) adsorption in Vijayaraghavan, K., Jegan, J., Palanivelu, K., & Velan, M. (2004). Removal of nickel(II) single and mixed system. Desalination and Water Treatment, 51, 7732–7745. ions from aqueous solution using crab shell particles in a packed bed up-flow column. Yang, Q., Tu, S., Wang, G., Liao, X., & Yan, X. (2012). Effectiveness of applying arsenate Journal of Hazardous Materials, 113(1-3), 223–230. reducing bacteria to enhance arsenic removal from polluted soils by Pteris vittata L. Vijayaraghavan, K., Joshi, U. M., & Balasubramanian, R. (2012). A field study to evaluate International Journal of Phytoremediation, 14,89–99. runoff quality from green roofs. Water Research, 46, 1337–1345. Yavuz, M., Gode, F., Pehlivan, E., Ozmert, S., & Sharma, Y. C. (2008). An economic re- Vijayaraghavan, K., Palanivelu, K., & Velan, M. (2006a). Treatment of nickel containing moval of Cu2+ and Cr3+ on the new adsorbents: Pumice and polyacrylonitrile/pu- electroplating effluents with Sargassum wightii biomass. Process Biochemistry, 41, mice composite. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 137, 853–859. 453–461. Vijayaraghavan, K., Palanivelu, K., & Velan, M. (2006b). Biosorption of copper(II) and Ye, J., Liu, C., Zhao, Z., Li, Y., & Yu, S. (2013). Heavy metals in plants and substrate from cobalt(II) from aqueous solutions by crab shell particles. Bioresource Technology simulated extensive green roofs. Ecological Engineering, 55,29–34. Reports, 97(12), 1411–1419. Yeo, C. K., & Tan, H. T. W. (2011). Ficus stranglers and Melastoma malabathricum: Vijayaraghavan, K., Jegan, J., Palanivelu, K., & Velan, M. (2005). Batch and column re- Potential tropical woody plants for phytoremediation of metals in wetlands. Nature in moval of copper from aqueous solution using a brown marine alga Turbinaria ornata. Singapore, 4, 213–226. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 106(2), 177–184. Yoon, J., Cao, X., Zhou, Q., & Ma, L. Q. (2006). Accumulation of Pb, Cu, and Zn in native Vijayaraghavan, K., Jegan, J., Palanivelu, K., & Velan, M. (2005). Biosorption of copper, plants growing on a contaminated Florida site. The Science of the Total Environment, cobalt and nickel by marine green alga Ulva reticulata in a packed column. 368, 456–464. Chemosphere, 60(3), 419–426. Zeng, Z., Zhang, S., Li, T., Zhao, F., He, Z., Zhao, H., et al. (2013). Sorption of ammonium Vijayaraghavan, K., Palanivelu, K., & Velan, M. (2005). Crab shell-based biosorption and phosphate from aqueous solution by biochar derived from phytoremediation technology for the treatment of nickel-bearing electroplating industrial effluents. plants. Journal of Zhejiang University Science B, 14, 1152–1161. Journal of Hazardous Materials, 119(1-3), 251–254. Zhang, M., Gao, B., Yao, Y., Xue, Y., & Inyang, M. (2012). Synthesis of porous MgO- Vilar, V. J. P., Botelho, C. M. S., & Boaventura, R. A. R. (2008). Lead uptake by algae biochar nanocomposites for removal of phosphate and nitrate from aqueous solu- Gelidium and composite material particles in a packed bed column. Chemical tions. Chemical Engineering Journal (Lausanne, Switzerland : 1996), 210,26–32. Engineering Journal (Lausanne, Switzerland : 1996), 144, 420–430. Zhang, Q., Miao, L., Wang, X., Liu, D., Zhu, L., Zhou, B., et al. (2015). The capacity of Vilar, V. J. P., Martins, R. J. E., Botelho, C. M. S., & Boaventura, R. A. R. (2009). Removal greening roof to reduce stormwater runoff and pollution. Landscape and Urban of Cu and Cr from an industrial effluent using a packed-bed column with algae Planning, 144, 142–150. Gelidium-derived material. Hydrometallurgy, 96,42–46. Zhang, X., Lin, L., Zhu, Z., Yang, X., Wang, Y., & An, Q. (2013). Colonization and mod- Volesky, B., Weber, J., & Park, J. M. (2003). Continuous-flow metal biosorption in a ulation of host growth and metal uptake by endophytic bacteria of Sedum alfredii. regenerable Sargassum column. Water Research, 37, 297–306. International Journal of Phytoremediation, 15,51–64. Wan, M.-W., Petrisor, I. G., Lai, H.-T., Kim, D., & Yen, T. F. (2004). Copper adsorption Zhang, Z., Szota, C., Fletcher, T. D., Williams, N. S. G., & Farrell, C. (2019). Green roof through chitosan immobilized on sand to demonstrate the feasibility for in situ soil storage capacity can be more important than evapotranspiration for retention per- decontamination. Carbohydrate Polymers, 55(3), 249–254. formance. Journal of Environmental Management, 232, 404–412. Wang, Z., Guo, H., Shen, F., Yang, G., Zhang, Y., Zeng, Y., et al. (2015). Biochar produced Ziogou, I., Michopoulos, A., Voulgari, V., & Zachariadis, T. (2018). Implementation of from oak sawdust by Lanthanum (La)-involved pyrolysis for adsorption of ammonium green roof technology in residential buildings and neighborhoods of Cyprus. + − 3- (NH4 ), nitrate (NO3 ), and phosphate (PO4 ). Chemosphere, 119, 646–653. Sustainable Cities and Society, 40, 233–243. Wenhao, Y., Hong, H., Mei, R., & Wuzhong, N. (2013). Changes of microbial properties in (near-) rhizosphere soils after phytoextraction by Sedum alfredii H: A rhizobox ap- proach with an artificial Cd-contaminated soil. Applied Soil Ecology : A Section of Futher reading Agriculture, Ecosystems & Environment, 72,14–21. Wong, G. K. L., & Jim, C. Y. (2014). Quantitative hydrologic performance of extensive Berardi, U., Ghaffarianhoseini, A., Ghaffarianhoseini, A., 2014. State-of-the-art analysis of – green roof under humid-tropical rainfall regime. Ecological Engineering, 70, 366 378. the environmental benefits of green roofs. ACS Applied Energy Materials 115, 411- Wong, N. H., Tay, S. F., Wong, R., Ong, C. L., & Sia, A. (2003). Life cycle cost analysis of 428. rooftop gardens in Singapore. Building and Environment, 38(3), 499–509. Yakkala, K., Yu, M.-R., Roh, H., Yang, J.-K., & Chang, Y.-Y. (2013). Buffalo weed

15