A Review of the Performance of Woody and Herbaceous Ornamental Plants for Phytoremediation in Urban Areas

Home , Helianthus annuus, Mirabilis jalapa

Review Article ii FF o o r r e e s s t t doi: 10.3832/ifor3242-013 Biogeosciences and Forestry vol. 13, pp. 139-151

A review of the performance of woody and herbaceous ornamental plants for phytoremediation in urban areas

Maurizio Capuana Urban and periurban areas are often contaminated by several pollutants. Phy- toremediation is considered to be an effective and eco-friendly strategy for the restoration of these contaminated lands. For this purpose, the exploitation of ornamental plants could be an additional option, due to their positive impact on the landscape. In this paper, we reviewed a selection of species which have been proposed for utilization in phytoremediation. Several tree species have been introduced in the past into urban environments for parks, gardens and avenues, with a selection studied for their capacity to absorb, tolerate, and translocate contaminants. Shrubby and herbaceous species are also commonly exploited for their ornamental features and are now studied for phytoremediation purposes. The responses of several effective species to the presence of heavy metals or dangerous organic compounds in the growth substrate are examined in this paper.

Keywords: Environment, Heavy Metals, Landscape, Organics, Pollution

Introduction lead is commonly found near roads and as- hold or translocate specific contaminants; Environmental pollution is an increasing sociated with zinc and cadmium (Garcia & moreover, these ornamentals pose little global problem. Contaminants vary de- Millan 1998); excessive copper is frequent- threat to food chain contamination, and pending upon their source and the type of ly detected in soils used for a long period can be appreciated by the resident popula- ecosystem involved. Urban areas can be af- as agricultural land, especially vineyards tions for their positive impact on land- fected by several organic and inorganic (Bretzel & Calderisi 2006), and chromium is scape. contaminants, which negatively impact a residual of some industrial activities (Za- In the more circumscribed field of flower- soils, water and the atmosphere (Biasioli et yad & Terry 2003). Organic pollutants can beds and urban green plantations, special al. 2006). The study of the effect of con- also injure urban soils by direct contamina- mixtures of topsoil are commonly used and tamination by pollutants on these urban tion, or after initial emission into the at- rules have to be followed with regards to environments and potential solutions to mosphere followed by transport in both the presence of contaminants (Huinink the problems associated with soil contami- gaseous and particulate forms, and subse- 1998). Risks are higher in allotments, since nation and rehabilitation dates to the last quent accumulation in soils after dry and contaminants could be transferred to the few decades (Tiller 1992). wet atmospheric deposition (Cachada et al. food chain (Scheyer 2000, Khalid et al. Urban and periurban soils are often pol- 2012). Urban soils may also be very differ- 2017). Attention has to be paid to parks, luted as consequence of human activities. ent to more natural soils, due to lower or- playgrounds, kindergartens and urban ar- Brownfield sites, mainly located in periur- ganic fraction, water drainage and aera- eas where people come into close contact ban sites, reflect industrial heritage and are tion, different pH value, microorganism with soil (Abrahams 2002, Chiesura 2004, probably the most common scenarios content and the presence of anthropic ma- De Miguel et al. 2006, Lee et al. 2006, Ljung where urban and periurban contaminated terial. These features can change the per- et al. 2006a, Ljung et al. 2006b). In these soils are found (Sleegers 2010). In general, formance of these soils with respect to pol- areas, selected ornamental plants may play heavy metals are the major contaminants: lutants (Tiller 1992, Schleu et al. 1998). As an important role in reducing the presence stated by Cunningham & Berti (1993) “new of pollutants, while at the same time giving technologies are needed to address nu- a pleasant temporary decoration. Botanists Institute of Biosciences and Bioresources, merous contaminants, especially those have elaborated several definitions of or- National Research Council, v. Madonna del Pi- that are neither volatile nor mobile in soil namental plants; these can be defined as ano 10, I-50019 Sesto Fiorentino, FI (Italy) solution”. Plants have been proposed to plants that have highly ornamental fea- mitigate the dangerous effects of pollu- tures such as ornamental flowers, fruits or @ Maurizio Capuana tants, with phytoremediation recognized foliage (Li & Zhou 2005). Nevertheless, we ([email protected]) as a promising technology for the recovery must also consider that the ornamental of contaminated environments (Salt et al. value of a plant may vary according to the Received: Sep 18, 2019 - Accepted: Feb 07, 1995). Phytoremediation could be success- different tastes and traditions of each 2020 fully exploited in urban territories; in these country. contexts, many herbaceous and some The focus of our attention is the “origi- Citation: Capuana M (2020). A review of the woody species (including forest species) nal” soils, and the present article is aimed performance of woody and herbaceous are suitable for planting because of their primarily at suburban areas, which can be ornamental plants for phytoremediation in ornamental features and adaptability to in- even heavily contaminated, due to their urban areas. iForest 13: 139-151. – doi: habited areas. Furthermore, plants are use- past uses. If the plants chosen to be used 10.3832/ifor3242-013 [online 2020-04-14] ful sensors to identify environmental con- in remediation are tree species, several se- tamination and potential exposures to pol- lection criteria have to be taken into ac- Communicated by: Werther Guidi Nissim lutants (Henry et al. 2013). In fact, some of count (Conway & Vander Vecht 2015), in- these species show the capacity to absorb, cluding problems linked to climate change

t Fig. 1 - In vitro culture for s

e the rapid mass propaga- r tion of plants to be o F

exploited in phytoremedia- d tion: (a) multiclonal culture n a of Populus alba; (b) in vitro-

s rooted plantlet of Salix e c alba. n e i c s o e g o i B

– t s e r o F i

(Roloff et al. 2009, Killi et al. 2018) and the plants (woody and herbaceous) must be Several tree species have been success- preferences expressed by the resident harvested and treated, since the content fully used in urban parks, gardens and av- populations (these inclinations are gener- of pollutants is an important concern. Sev- enues; for instance, in Europe pines, cy- ally for plantations with high level of biodi- eral solutions are available for this pur- presses, poplars, willows, birches, syca- versity – Carrus et al. 2015). Also, it is al- pose, including compacting, composting, mores and lindens are widely planted (Mil- ways advisable to consider all of the ac- biogas production and pyrolysis (Blaylock ler et al. 2015). Numerous recent studies tions related to the sustainability of planta- & Huang 2000, Nanda Kumar et al. 1995, demonstrated that some tree species have tions (Ferrini & Fini 2011) and the analysis of Garbisu & Alkorta 2001). The easiest proce- a good attitude to tolerate, absorb and re- costs for their periodic removal and dis- dure is incineration of biomass, with recov- move specific contaminants from the soil posal (Berndes et al. 2004, Lewandowski et ery of residual heavy metals. When orna- (reviewed by Mahar et al. 2016, Pajević et al. 2006, Compernolle et al. 2012, Saxena et mental flowers are used, cut flowers with al. 2016). Trees can enhance the aesthetic al. 2019, Wan et al. 2016). limited contaminants content can be even- quality of urban landscape (Chen et al. In this context, we might also consider tually sold. 2009), simultaneously providing other the possible use of tree planting for short- An overview is provided of the most ef- functions, such as improved air quality rotation coppicing, by which a profitable fective woody and herbaceous plants (tree (Mukherjee & Agrawal 2018), reduction of recovery of the used plants can be per- species, shrubs and herbaceous flowers) noise pollution (Pathak et al. 2011), mitiga- formed. For instance, willows may be ex- for the remediation of urban and suburban tion of waterlogging (Livesley et al. 2016) ploited for this purpose, since these spe- areas, through analysis of recent literature and reducing heat island effects (Scholz et cies display high ornamental value and are illustrating how these species react when al. 2018 – Fig. 1, Fig. 2). suitable for bioenergy production com- facing either inorganic (heavy metals) or A great variety of herbaceous and bined with potential for phytoremediation organic contaminants. This review is specif- shrubby species have been analysed for (Guidi et al. 2013, Guidi Nissim et al. 2014b). ically addressed to a selection of species phytoremediation purposes (reviewed by Therefore, the choice of species to be used suitable for exploitation in urban environ- Liu et al. 2018 – Fig. 3), but many still re- for phytoremediation includes considera- ments, due to their adaptability, ornamen- main to be studied. Furthermore, plants’ tion of criteria such as respect for biodiver- tal characteristics and appreciation by resi- association, with its huge possibilities of sity, easy harvesting management, by- dent populations; the proposed selection, combinations, offers interesting perspec- product utilisation and possible economic albeit large, is mainly focused on the spe- tives and is therefore discussed. returns. cies best suited to European and American The choice of ornamental woody and After their use for soil remediation, all environments. herbaceous plants for urban (and periur-

Fig. 2 - Woody species for phytoremediation: (a) a poplar plantation in an urban site (outskirts of Flo- rence); (b) Betula pendula.

140 iForest 13: 139-151 Phytoremediation in urban areas y r

Fig. 3 - Two widespread t s

ornamental species studied e and proposed for phytore- r o F

mediation purposes: (a)

Chrysanthemum; (b) Ner- d n

ium oleander. a

s e c n e i c s o e g o i B

–

t s e r o F i ban) environments should also take into duction of biomass, easy propagation, a and Schizolobium parahyba, were tested in account some factors. In these sites (often deep root system and the capacity to up- a lead-contaminated area. While M. caesal- smaller areas compared to the country- take and translocate a significant amount piniaefolia did not show symptoms of Pb side), the problem of the scattering of of metal contaminants in the soil to the toxicity, the other two species exhibited leaves could be more relevant; especially shoots (Vassilev et al. 2004, Guerra et al. reduced shoot biomass yield, leaf area and when using trees, and for species that 2011). Poplars in particular, display a num- height. The increase of Pb concentrations translocate pollutants to the leaves, leaves ber of different characteristics useful to- in soil led to augmented Pb concentration should be periodically collected and wards environmental protection, which in- in shoots and roots, but most of the Pb ac- treated. Moreover, due to the greater an- clude phytoremediation, especially in com- cumulated in the roots, and only a small thropic presence in urban site and trans- bination with short rotation forestry and fraction was translocated to the above- port constraints, it is probably opportune landscape restoration (Facciotto et al. ground parts of the plant. Mimosa showed to choose species that have less mainte- 2014). Woody species may also be utilised the highest Pb tolerance and phytostabili- nance needs and leaves which are easier to for the plantation of green belts around sation potential in lead-contaminated soils collect at the end of the leaf life-cycle. contaminated lands. Eucalypts, willows (Ribeiro De Souza et al. 2012). and poplars are all fast-growing trees with In a study to identify candidate species Heavy metals short rotation coppice systems that could among fast-growing trees for remediating Pollution from industrial emissions, efflu- be successfully utilised for this purpose Pb-contaminated soils (Yongpisanphop et ents and solid discharges are the main (Pulford & Watson 2003). This phytoreme- al. 2017), hydroponic cultures of cuttings source of an abnormal high presence of diation would have to be undertaken in from Acacia mangium, Azadirachta indica, heavy metals in soils. In general, numerous consideration of the need to harmonize Eucalyptus camaldulensis, and Senna sia- human activities result in the emission of these choices with the landscape charac- mea, were tested in increasing Pb concen- these harmful pollutants that enter into ter, as generally requested by the resident trations. All species showed high Pb toler- the biosphere through wastes (emission, populations (Boll et al. 2014). ance (over 78%) but low TF (<1) for all treat- waste-water and waste solid), including The effect of lead (Pb) has been assessed ments (10, 30, and 50 mg L-1). Based on municipal wastes in agriculture and exces- in one-year-old potted seedlings of Cap- these indices, A. mangium and E. camaldu- sive use of fertilizers. Several plant species padocian maple (Acer cappadocicum), Eu- lensis were found to be good candidate have the capacity to absorb and translo- ropean ash (Fraxinus excelsior) and Orien- species for Pb remediation (Yongpisan- cate specific metals; a selection of woody tal aborvitae (Platycladus orientalis). In- phop et al. 2017). and herbaceous species, which could be creasing Pb application in the soil (from Willow (Salix nigra) showed a moderate identified as “multipurpose species”, are 100 to 500 mg kg-1) did not affect the dry tolerance to silver (Ag) in a hydroponic ex- reviewed below, for their possible utilisa- weight of roots of all species, while a grad- periment with increasing AgNO3 concentration in metal remediation coupled to con- ual decrease was detected in leaves and tions, observing a significant reduction of siderable ornamental features (Tab. 1, Tab. shoots, with the highest inhibition in P. ori- biomass production with AgNO3 0.027 μM, 2). entalis. This species, however, showed the but also adaptation signals over a longer highest translocation factor values, toler- timeline (Guidi Nissim et al. 2014a). Woody species ance index and bioconcentration factor, in- Eastern cottonwood (Populus deltoides) Among tree species traditionally used in dicating a possible use of this conifer spe- was evaluated for arsenic (As) tolerance urban and periurban plantations, a limited cies for remediation of Pb-polluted soils and phytostabilization potential, by expo- number showed suitability for phytoreme- (Abbasi et al. 2017). The bioconcentration sure to various As levels in soil (control, 5, diation purposes. Analysis of the recent lit- factor (BF) is defined as the ratio of met- 10, 15, and 20 mg kg-1) in a 9-month pot ex- erature indicates that the most promising al(loid) concentration in aerial biomass to periment. Plant height stress tolerance in- are some species of the Salicaceae family that in soil, and the translocation factor dex (TI) significantly decreased with in- (Salix spp., Populus spp.), but some others (TF) the ratio of metal(loid) concentration creasing As levels, while indices related to also show significant pollution resistance in shoots to that in roots, both factors tak- root length and dry matter were not af- traits, such as Ailanthus altissima, Robinia ing values >1 in accumulators and <1 in ex- fected. TF and BF were less than 1.0, but pseudoacacia, Betula pendula, Carpinus be- cluders; the tolerance index (TI) is the per- root and shoot As content significantly in- tulus, Ginkgo biloba and Platanus hispanica cent of the organ’s growth of the treated creased with increasing As concentrations (Dadea et al. 2017). Several tree species plant compared to the growth of the con- (Hussain et al. 2017). The effect of high cop- (mainly willows and poplars) are not hyper- trol plant (McGrath & Zhao 2003, Turner et per (Cu) concentrations was investigated accumulators, but do exhibit traits of high al. 1991). Three leguminous woody species, on poplar woody cuttings (Populus × eu- interest, such as fast growth and high pro- Mimosa caesalpiniaefolia, Erythrina speciosa ramericana, clone “Adda”), finding that in- iForest 13: 139-151 141 Capuana M - iForest 13: 139-151 y

r tent in the roots of Rhapis excelsa was the

t Tab. 1 - Ornamental plants for the phytoremediation of heavy metal: trees and shrubs.

s highest amongst all the tested species and

e (A): accumulation; (T): translocation. -1

r 7.05 times higher than that at 10 mg kg Cd o concentration (Zhang et al. 2010). Lonicera F Group Species Pollutants A / T References japonica plants exposed to Cd concentra- d -1 n Acacia mangium Pb A Yongpisanphop et al. 2017 tions up to 50 mg L did not show signifi- a Acer cappadocicum Pb A Abbasi et al. 2017 cant differences (compared to control) in s e Azadirachta indica Pb A Yongpisanphop et al. 2017 height and dry biomass of leaves and c n Betula pendula Zn A,T (partial) Rosselli et al. 2003 roots. TIs were all above 0.8 and the high e i Cinnamomum camphora Zn A,T Zeng et al. 2018 BF and TF justified the proposal to include c

s the species in the list of potential Cd accu- Eucalyptus Pb A Yongpisanphop et al. 2017, o mulators (Liu et al. 2009). e camaldulensis Cd T Motesharezadeh et al. 2017 g The ornamental shrub Euphorbia milii tol- o Fraxinus excelsior Pb A Abbasi et al. 2017 i erated up to 75 mg of applied Cr per Kg

B Mimosa cesalpiniaefolia Pb A Abbasi et al. 2017 soil, and was efficient in translocating Cr – Platycladus orientalis Pb T Abbasi et al. 2017 from roots to shoots. Plant death occurred t s Populus alba Cd,Pb A Houda et al. 2016, Zacchini when higher metal concentrations were e r et al. 2009 used (Ramana et al. 2015). o

F Populus deltoides As A Hussain et al. 2017 Buddleja asiatica is known to display a i Cd A Zacchini et al. 2009 high accumulation capacity and tolerance

s Populus nigra Cd A Zacchini et al. 2009 for lead. This species, and the related orna- e e r Populus trichocarpa Cd A Zacchini et al. 2009 mental B. paniculata, were therefore inves- T Populus × canadensis Cd A Zacchini et al. 2009 tigated in a hydroponic culture, in the pres- -1 Populus × euramericana Cu A Borghi et al. 2007 ence of 10 or 20 mg L Pb. Both species Zn T (partial) Di Baccio et al. 2003 showed increased biomass and Pb concentrations in the roots of 12.1 and 21.7 mg kg -1, Cr, Fe T (partial) Giachetti & Sebastiani 2006 respectively. In a 3-month pot experiment, Populus × generosa Cd A Zacchini et al. 2009 using three different soils with various Pb Salix dasyclados Cd A Landberg & Greger 1994 levels (10.6, 31.3, and 89.1 mg kg-1) the two Zn T Vyslouzilová et al. 2003 species of Buddleja had a slight decrease in Salix fragilis Cd, Zn T Meers et al. 2007 survival rates at the highest Pb concentra- Salix miyabeana Zn T Desjardins et al. 2016 tion, but a general regular growth. In a 6- Salix nigra Ag A Guidi Nissim et al. 2014b month field trial experiment conducted in Salix schwerinii Cd, Zn T Meers et al. 2007 Pb-contaminated sites (Pb content: 95-101 -1 Salix viminalis Cd A Landberg & Greger 1994 mg kg ), both Buddleja species showed Zn T Vyslouzilová et al. 2003 100% survival, increased biomass produc- Senna siamea Pb A Yongpisanphop et al. 2017 tion and phytoextraction capacity (TF) from 1.1 to 2.3 (Waranusantigul et al. 2008). Buddleja asiatica Pb T Waranusantigul et al. 2008 Ricinus communis, as well, showed the ca- Buddleja paniculata Pb T Waranusantigul et al. 2008 pacity to uptake nichel (Ni) from contami- Catharanthus roseus Ni, Pb A Subhashini & Swamy 2013 nated soils, and was therefore classified as Euonimus japonicus Cd A Zeng et al. 2018 an accumulator (Adhikari & Kumar 2012); Euphorbia milii Cr T Ramana et al. 2015 this species also demonstrated a great po-

s Ligustrum vicaryi Cd A Zeng et al. 2018

b tential for Cd removal, due to its features u r Lonicera japonica Cd T Liu et al. 2009 of fast growth, high biomass and consider- h S Loropetalum chinense Cd A Zeng et al. 2018 able absorption and accumulation (Huang Osmanthus fragrans Cd A, T Zeng et al. 2018, Wu et al. et al. 2011). 2011 It is more common for a soil to be af- Pb T Wu et al. 2011 fected by the pollution of a mix of heavy Rhapis excelsa Cd A Zhang et al. 2010 metals; some case studies are therefore re- Ricinus communis Ni A Adhikari & Kumar 2012 ported below concerning woody plants. In a pot experiment with seven willow clones, significant differences between creasing levels of Cu up to 100 μM resulted grans, Ligustrum vicaryi, Loropetalum chi- clones were found in cadmium and zinc ac- in a general reduction of plant growth and nense var. rubrum, and Euonymus japonicus cumulation. Cd and Zn were transferred that the metal was mainly accumulated in cv. Aureo-mar) were tested in the presence from roots to aboveground tissues (mainly the root system at all Cu levels (Borghi et of Cd. The results showed that these spe- leaves), leading to the conclusion that wil- al. 2007). Several poplar species (Populus cies can grow normally at Cd soil concen- lows are suitable phytoextractors of mod- alba, P. deltoides, P. nigra, P. trichocarpa, P. trations lower than 24.6 mg kg-1. The metal erately contaminated soils (Vyslouzilová et × generosa, P × canadensis) showed the ca- accumulated principally in the roots, with al. 2003). Another study tested the ability pacity to accumulate cadmium (Cd), albeit the highest amount detected in Euomymus of five woody species to extract heavy with different effectiveness (Zacchini et al. (Zeng et al. 2018). metals (copper, zinc or cadmium) from a 2009). Poplars also demonstrated phytoex- Rhapis excelsa, Camellia polyodonta and C. polluted soil. Salix viminalis and Betula pen- traction capacity for zinc (Zn – Di Baccio et gigantocarpa were tested for soil Cd ab- dula had already demonstrated phytoex- al. 2003). sorption in a pot experiment with different traction ability for Zn and Cd, while the Cadmium accumulation was also demon- Cd treatments (10, 25 and 50 mg kg-1). The phytoextraction capabilities of Alnus inca- strated in Cinnamomum camphora, that three species never showed any toxic na, Fraxinus excelsior and Sorbus mougeotii showed the maximum Cd content in stems symptom and grew well at all Cd concen- were unknown. The results suggest that and leaves (Zeng et al. 2018). trations. Cadmium contents was higher in none of these species transferred Cu to the In a greenhouse experiment on ornamen- the roots than in the stems and leaves. At shoots. Salix and Betula were able to trans- tal plants, four shrubs (Osmanthus fra- 50 mg kg-1 Cd concentration, the Cd con- fer Zn and Cd to leaves and twigs, while Al-

142 iForest 13: 139-151 Phytoremediation in urban areas y

nus, Fraxinus and Sorbus excluded them r

Tab. 2 - Ornamental plants for the phytoremediation of heavy metals: herbaceous t

from their above-ground tissues (Rosselli s

species. (A): accumulation; (T): translocation. e

et al. 2003). A pot experiment involving r

Salix miyabeana grown in brownfield soils o F differentially contaminated with Ag, Cu Group Species Pollutants A / T References d and Zn (up to 113.60, 47.50, and 117.00 mg Althaea rosea Cd T Liu et al. 2008 n

-1 a kg respectively), demonstrated a potential Pb A Liu et al. 2008 s capability for phytoremediation, since a Alternanthera Cd, Pb T Tauqeer et al. 2016 e c

high concentration of Zn (119.96 ± 20.04 bettzickiana n

-1 e mg kg ) was detected in above-ground Alyssum maritima Cr T Budak et al. 2011 i c plant tissues at the end of the treatment Amaranthus caudatus Ni T Bosiacki & Wojciechowska s (Desjardins et al. 2016). o

2012 e

Five species of Salix were tested in a pot Cd T Cay 2016 g o experiment to compare their capacity to Aptenia cordifolia Cr T (partial) Budak et al. 2011 i B extract and accumulate Cd, Zn, Cu, Ni, Pb,

Calendula officinalis Cd A Liu et al. 2008 – and chromium (Cr). Salix schwerinii Cr T (partial) Ramana et al. 2013 t “Christina”, S. dasyclados “Loden” and S. s Cu T Goswami & Das 2016 e fragilis “Belgisch Rood” showed the high- r Canna indica Pb, Zn Cr, T Subhashini & Swamy 2014 o est Cd and Zn accumulation and were F therefore considered good candidates for Ni, Cd A Subhashini & Swamy 2014 i remediation (Meers et al. 2007). In an ex- Chlorophytum comosum Cd T Wang et al. 2012 periment on a strongly polluted soil (up to Zn T Tao et al. 2011 18 mg Cd kg-1, 1400 mg Cu kg-1, 500 mg Pb Gomphrena globosa As A Signes-Pastor et al. 2015 kg-1 and 3300 mg Zn kg-1), Salix viminalis Helianthus annuus Cu T Forte & Mutiti 2017 demonstrated a high translocation of Cd Cd T Bosiacki 2008 -1 -1 (≥80 mg kg ) and zinc (≥3000 mg kg ) to s

u Ni T Mohammadzadeh et al. 2014 o the leaves alongside reduced growth. In e As T Reed et al. 2013 c contrast, when grown in a moderately pol- a

b Hydrangea paniculata Cu T Forte & Mutiti 2017

-1 r

luted soil (2.5 mg Cd kg and 400 mg Zn e

H Impatiens balsamina Cr T (partial) Miao & Yan 2013 kg-1), S. viminalis extracted 0.13% of total Cd and 0.29% of total Zn per year and exhib- Iris lactea Cd A Han et al. 2007 ited vigorous growth (Jensen et al. 2009). Iris pseudacorus Cr, Zn A Caldelas et al. 2012 In another study on eight Salix viminalis Mesembryanthemum Ni T (partial) Amari et al. 2016 clones and one S. alba clone, differences crystallinum emerged between clones in biomass pro- Mirabilis jalapa Cr T Miao & Yan 2013 duction and accumulation efficiency, with Salvia splendens Cd T Bosiacki 2008 two S. viminalis clones demonstrating a su- Polianthe tuberosa Cd T Ramana et al. 2012 perior capacity to accumulate five heavy Pteris vittata As T Zeng et al. 2019 metals (Cd, Cu, Hg, Pb, Zn – Mleczek et al. Sedum alfredii Zn A Cheng & Zhou 2014 2010). Syngonium sp. As A Huq et al. 2005 Poplars also showed some potential for Tagetes erecta Cd A Bosiacki 2008 phytoextraction of chromium and iron (Gi- Ni T Bosiacki & Wojciechowska achetti & Sebastiani 2006), cadmium and 2012 lead (Houda et al. 2016). As T Reed et al. 2013 The accumulation of heavy metals has Tagetes patula As A Huq et al. 2005 been assessed in leaves of some ornamen- Tagetes erecta patula As T Chintakovid et al. 2008 tal trees and shrubs used in districts of Tur- × key affected by high heavy metal pollution, Vinca rosea Cr T Ehsan et al. 2016a finding significant differences among the Zinnia elegans Pb, Cr T Ehsan et al. 2016b tested species. The highest concentrations As A Signes-Pastor et al. 2015 (mg kg-1) of Zn, Cu, Cd and iron (Fe) were observed in Cedrus libani (618.0), Betula alba (106.3), Salix alba (24.5) and Eleagnus plants, Tagetes erecta, Salvia splendens, and found in roots, then in leaves and shoots, angustifolia (0.3), while the highest Ni (6.4) Abelmoschus manihot, finding a little effect and the lowest in inflorescences (Bosiacki and Pb (3.8) contents were found in Pyra- on seed germination of the three species 2008). Five concentrations of Cd (0, 25, 50, cantha coccinea (Gülser et al. 2011). and on shoot elongation of S. splendens, 75 and 100 mg kg-1 soil) were tested with A pot experiment was carried out on os- but a significant inhibitory effect on root three varieties of tuberose, finding that manthus (Osmanthus fragrans var. thun- elongation of all the tested plants and on this metal did not produce any toxic macro- bergii), cultured in substrate supplemented shoot elongation of T. erecta. The calcu- scopic symptoms in all the three varieties. with different concentrations of Cd, Pb, Zn, lated Cd-tolerance indices led to the con- Having shown Cd accumulation in the and Cu. The species showed high Cd and clusion that A. manihot was the most toler- shoots higher than 100 μg g-1 dry weight Pb transfer efficiencies and a limited trans- ant plant to Cd while S. splendens the most and a ratio of Cd >1 in the shoots to bulbs, fer of Zn and Cu in the presence of Cd, sug- sensitive (Wang & Zhou 2005). Conversely, this species has to be considered as a po- gesting the possible utilization of osman- Bosiacki (2008) found high Cd accumula- tential effective Cd accumulator (Ramana thus in phytoremediation applications (Wu tion in leaves and shoots of Salvia splen- et al. 2012). Chlorophytum comosum is a po- et al. 2011). dens, as well as in inflorescences of He- tential Cd accumulator; in a pot experiment lianthus annuus, which is one of the most it showed a TI above 100 in soil Cd concen- Herbaceous species studied ornamental species for remedia- tration of 100 mg kg-1, and at Cd concentra- Cadmium is one of the most widespread tion purposes, while Tagetes erecta proved tion up to 200 mg kg-1, the Cd content in contaminating metals in soils. Its action a moderate capacity to extract and accu- roots and aboveground tissues reached was investigated on three ornamental mulate Cd, with the greatest amount 1522 and 865 mg kg-1, respectively (Wang et iForest 13: 139-151 143 Capuana M - iForest 13: 139-151 y

r al. 2012). A detailed work on the relation roots of Brassica juncea (Budak et al. 2011). sis showed respectively 85% and 65% reduc-

t -1

s between Canna indica and Cd, demon- In a study on exposure to Cr of four orna- tions in dry weight at 0.75 mg L As concen- e

r strated its considerable potential in cad- mental plants, calendula, chrysanthemum, tration. At the highest As rate, marigold o mium accumulation, but the root concen- aster and dahlia, the metal caused a drastic and sunflower had uptake ratios of 7.4 and F tration factor was higher than the BF, indi- reduction of plant growth at 10 mg kg-1, 16.6, respectively, and TF near one, allow- d -1 n cating a limited translocation (Solanki et al. and at 25 mg kg was responsible of a dif- ing consideration of these species as inter- a 2018). Calendula officinalis was found to fuse mortality in chrysanthemum. Overall, esting candidates for As phytoremediation s e grow normally in soils containing 100 mg only calendula could be considered a possi- (Reed et al. 2013). c -1

n kg Cd, with high metal accumulation in ble candidate for phytoremediation of soils The effects of As were tested under hy- e i roots and shoots. In a hydroponic culture, contaminated with low level of Cr (Ramana droponic conditions on two other flower- c

s for Althaea rosea the highest Cd accumula- et al. 2013). In another experiment on three ing species, Gomphrena globosa and Zinnia o tion was detected in shoots, and for both ornamental species cultured in pots con- elegans. Arsenic principally accumulated in e g Calendula officinalis and Althaea rosea, a taining substrate with four Cr concentra- the roots, followed by leaves, stems and o i good accumulation capacity and tolerance tions, Impatiens balsamina showed a de- flowers, indicating that these species were B to Pb were also observed (Liu et al. 2008). cline in the biomass as the dose of Cr in- arsenic tolerant plants but not potentially – Iris lactea var. chinensis was found to accu- creased, while in Mirabilis jalapa and Tage- As-remediating (Signes-Pastor et al. 2015). t s mulate Cd in leaves and roots after treat- tes erecta the four treatments did not im- For the phytoremediation of mixed heavy e r ment with a hydroponic culture with 0 to pact growth; TF and BF of M. jalapa were metals, a study on Alternanthera bettzick- o -1

F 160 mg L Cd treatment, showing a TI greater than 1, indicating this species is a iana, a species commonly used as an orna- i higher than the value detected in the other good candidate for the remediation of Cr- mental edging plant, showed a good accu- species tested, I. tectorum (Han et al. polluted soils (Miao & Yan 2013). In Vinca mulation of Cd and Pb at concentrations up 2007). rosea grown in pots containing soil with to 1.0 mM, with total uptake of both met- The effects of increasing doses of Ni (up levels of chromium from 10 to 60 mg kg-1, als higher in shoots than roots (Tauqeer et to 300 mg dm-3 substrate) were investi- plant height, fresh and dry weight de- al. 2016). Based on BF and TF, also Canna gated in three selected ornamental plants: creased with high contamination levels of indica was indicated to be a good accumu- Tagetes erecta, Helianthus annuus, and chromium. TFs were found to be lower lator of Cd, Pb, Ni, Zn, and Cr, with high TF Amaranthus caudatus, finding that the than 1 for low metal concentrations and for Ni and Cr (Subhashini & Swamy 2014). highest amounts of Ni were accumulated higher than 1 with Cr concentrations from The macrophyte Iris pseudacorus is consid- in leaves of tagetes and amaranth, and in 30 to 60 mg kg-1 (Ehsan et al. 2016a). ered to be a candidate for Cr rhizofiltration inflorescences of sunflower. Globally, tage- In the presence of Pb, the remediation and Zn phytoextraction, having shown a tes showed the highest Ni uptake at con- potential of Vinca rosea was higher than 1 good tolerance and accumulation capacity centrations of 25 and 50 mg dm-3, while for at Pb concentrations from 20 to 40 mg kg-1 towards these two metals. Plants grown in -1 the substrates with an addition of 75, 150 and lower with 50 to 90 mg kg (Ehsan et a nutrient solution containing ZnCl2 or CrCl3 or 300 mg Ni dm-3, the greatest accumula- al. 2016b). Similar results were obtained from 0 to 200 μg ml-1 survived and accumu- tion was recorded in amaranth (Bosiacki & with zinnia (Zinnia elegans) grown in pots lated Cr and Zn in all tissues (Caldelas et al. Wojciechowska 2012). An interesting orna- containing soils with different levels of 2012). In a greenhouse experiment, Hydran- mental halophyte, Mesembryanthemum lead and chromium. Plants grown in the gea paniculata and Helianthus annuus accu- crystallinum, was compared to the model presence of lead were healthier compared mulated significant amounts of Cu and Pb. species Brassica juncea, growing the plants to plants grown in Cr-contaminated soils. Helianthus showed high accumulation of for 3 months on a soil containing 0, 25, 50, TF was also higher in Pb-contaminated soils heavy metals in the shoots and efficacious -1 and 100 mg kg NiCl2. Ni reduced the (Ehsan et al. 2016c). translocation to the leaves, while Pb was growth activity of both species, but to a For copper remediation, Calendula offici- not as easily taken up and translocated as lower extent in M. crystallinum. Ni accumu- nalis showed a high tolerance (up to 400 Cu. Hydrangea stored more metals in stems lated mainly in roots and the fraction mg kg-1) to copper contamination, with the than in leaves, showing a lower transloca- translocated to shoots was higher in M. maximum Cu accumulation (4.67 and 3.99 tion ability than Helianthus (Forte & Mutiti crystallinum than in B. juncea (Amari et al. mg g-1 in leaves and roots, respectively) in 2017). Tanacetum vulgare showed environ- 2016). Catharanthus roseus irrigated for 60 soil treated with 300 mg Kg-1, a level con- mental adaptability on high industrial pollu- days with aqueous solutions of nickel and siderably higher than the amount of 1 mg tion and an interesting capacity of mercure lead showed high accumulation of the two g-1 which defines Cu hyperaccumulators and lead uptake (Stevović et al. 2010). metals by roots, and to a lesser extent in (even the TF was >1 at all Cu doses – Gos- stems and leaves (Subhashini & Swamy wami & Das 2016). Organics 2013). For arsenic remediation, Tagetes patula Phytoremediation of organic contami- Chlorophytum comosum seedlings treated and Syngonium sp. were tested in pots nants generally involves few classes of with Zn showed inhibition of root length with soil containing As up to 10 mg kg-1. The compounds, which are principally chlori- and fresh and dried plant weight at all the plants showed significant As accumulation, nated solvents, petroleum hydrocarbons tested Zn concentrations (from 200 to particularly in roots, with an average TF of (PHCs), polycyclic aromatic hydrocarbons 2000 mg kg-1), while the length of above- 0.91 for marigold and 0.75 for arum (Huq et (PAHs), polychlorinated biphenyls (PCBs) ground tissues and the volume of roots de- al. 2005). A further experiment on a and explosives. Contamination of soils with clined with the Zn dose. TI was above 50 at triploid hybrid Tagetes erecta × patula such products can have several causes, the Zn concentrations lower than 600 mg kg-1 showed that arsenic was found mostly in main ones being uncontrolled industrial ac- (Tao et al. 2011). leaves (46.2%) with the lowest As content tivity, intensive farmland exploitation and Aptenia cordifolia, Brassica juncea, Bras- (5.8%) in flowers. The hybrid plants contin- percolation of polluted waters of various sica oleracea, and Alyssum maritima were ued to grow vigorously in the As-contami- origins. The most common contaminated studied for their capacity to uptake and nated substrate (Chintakovid et al. 2008). soils are probably former industrial sites, translocate hexavalent chromium (VI) sup- Several ornamental plant species were which may display residual pollutants at plied by irrigation. Increases in the Cr con- tested for their potential for As remedia- different soil depths. centration significantly enhanced both action in a hydroponic system: iris (Iris savan- Over recent years, positive results have cumulation and translocation of the metal narum), switchgrass (Panicum virgatum), emerged regarding the capacities of sev- in the roots and shoots of the tested spe- Tithonia rotundiflora, Coreopsis lanceolata, eral plant species to degrade specific or- cies, with highest values recorded in the sunflower (Helianthus annuus), and mari- ganic compounds. According to Shimp et shoots of Alyssum maritima and in the gold (Tagetes erecta). Tithonia and Coreop- al. (1993) it is fundamental to understand

144 iForest 13: 139-151 Phytoremediation in urban areas y

the physical, biological, and chemical rela- r

Tab. 3 - Ornamental plants for the phytoremediation of organic compounds. (B[a]P): t

tionships that determine the fate of each s

benzo[a]pyrene; (DDT): dichlorodiphenyltrichloroethane; (HCH): hexachlorocyclohex- e

organic contaminant in the rhizosphere. r ane; (PCB): polychlorinated biphenyls; (PAH): polycyclic aromatic hydrocarbons; In this section some case examples con- o F cerning ornamental woody and herba- (TCE): trichloroethylene; (TPH): total petroleum hydrocarbons. d ceous species are illustrated (Tab. 3). n a

Group Species Pollutants References s

Woody species Itea virginica Oryzalin Baz & Fernandez 2002 e c

In a soil contaminated with a mix of Populus deltoides × nigra TCE Doty et al. 2017 n e PAHs, PCBs and heavy metals, two clones Dioxane Aitchison et al. 2000 i c

of different willow species (Salix sachali- s PCB Liu & Schnoor 2008 o s

nensis SX61 and S. miyabeana SX64) gave e e

e Atrazine Burken & Schnoor 1997 r encouraging growth and survival results af- g T o ter a single growing season planted in soils Populus hybrids HCH Bianconi et al. 2011 i B with high concentrations of both organic Salix alba Oryzalin Baz & Fernandez 2002 – and heavy metal contaminants (Guidi et al.

Salix miyabeana PAH, PCB Guidi et al. 2012 t

2012). Salix alba, S. gracilistyla var. melanos- s

Salix sachalinensis PAH, PCB Guidi et al. 2012 e tachys and Itea virginica were treated for 9 r s -1 Cytisus striatus HCH Becerra-Castro et al. 2013 o b days with a 4 mg L suspension of two her- F u i

r Nerium oleander Fluoride Khandare et al. 2017 bicides (isoxaben and oryzalin). Isoxaben h reduced the growth rate of white willow S Ricinus communis DDT Huang et al. 2011 and I. virginica, while both herbicides re- Aloe vera Formaldehyde Liu et al. 2007 duced the growth index for S. gracilistyla. Aster amellus Dyes Khandare et al. 2011 The final dry weight was lower for all taxa Canna indica Triazophos Cheng et al. 2007 when exposed to both herbicides, but the Chrisanthemum morifolium Benzene, Liu et al. 2007 set of data suggest that S. alba and I. vir- Formaldehyde ginica display some attitude in the remedia- Crassula portulacea Benzene Liu et al. 2007 tion of oryzalin (Baz & Fernandez 2002). Dianthus chinensis Sulfur dioxide Liu et al. 2007 In hydroponic studies, hybrid poplar cut- Echinacea purpurea TPH Liu et al. 2012 tings (Populus deltoides × nigra) removed s u

o Festuca arundinacea TPH Liu et al. 2012

54.0% of dioxane (1,4-Dioxane), a persistent e c Gaillardia aristata TPH Liu et al. 2012 environmental pollutant, indicating the po- a b r Gaillardia grandiflora Dyes Chandanshive et al. 2018 tential of this species in the phytoremedia- e tion of sites contaminated by dioxane and H Impatiens balsamina TPH Cai et al. 2010 other hydrophilic pollutants (Aitchison et Iris lactea TPH Cheng et al. 2017 al. 2000). P. deltoides × nigra showed also Medicago sativa TPH Liu et al. 2012 the capacity to accumulate PCBs, observ- Mirabilis jalapa B[a]P Sun & Zhou 2016 ing that mono- and di-chlorinated congeners were primarily translocated from Portulaca grandiflora Dyes Chandanshive et al. 2018 the roots to the secondary stems, tri-chlori- Portulaca oleracea Fluoride Khandare et al. 2017 nated to the main stem but not farther, Tagetes patula Dyes Chandanshive et al. 2018 and tetra-chlorinated were bound strongly B[a]P Sun & Zhou 2016 to root tissues (Liu & Schnoor 2008). With the same hybrid, the capacity to uptake, hydrolyze and dealkylate atrazine to less observed, suggesting that these ornamen- dichotoma tolerated lower PHC concentra- toxic metabolites was detected by Burken tal species could be an interesting solution tions, with a lower rate of total petroleum & Schnoor (1997). for use on the ridges of constructed wet- hydrocarbons (TPHs) degradation (Cheng Nerium oleander (Fig. 3b) resulted able to land for the treatment of dyes (Chandan- et al. 2017). Impatiens balsamina was also remove 92% of fluoride from a 10 mg L-1 NaF shive et al. 2018). tested for petroleum remediation, finding solution, within 15 days (Khandare et al. Tagetes patula and Mirabilis jalapa were that after a 4-month culture period in pot, 2017). Ricinus communis showed a great tested in a pot experiments to evaluate the average TPHs degradation rate was up potential for removing dichlorodiphenyl- their remediation capacity towards ben- to 18.13-65.03%, greater than that (10.20- trichloroethane (DDT) from contaminated zo[a]pyrene (B[a]P). The dry biomass of 35.61%) of natural degradation in the con- soils, with different effectiveness depend- the two species increased at low B[a]P trol treatment (Cai et al. 2010). ing on the genotype (Huang et al. 2011). doses and then reduced with increasing In a pot-culture experiment to assess the concentrations. It also emerged that the TPHs-phytoremediation potential of 14 or- Herbaceous species tolerance to this pollutant was greater at namental plants in petroleum-contami- In a study on Aster amellus, the capacity the plant’s flowering and mature stages nated soil, it emerged that Gaillardia aris- was observed to decolorize the sulfonated compared with the seedling stage. Signifi- tata, Echinacea purpurea, Festuca arundi- azo dye Remazol Red. After the cultivation cantly positive correlations were found be- nacea and Medicago sativa were effective in period, four non-toxic metabolites were tween the B[a]P content of roots, stems, reducing TPHs (and related compounds) in identified; this indicated that the plant can leaves and shoots to soil B[a]P concentra- 10 mg kg-1 TPH-contaminated soil. Removal be used for cleaning textile effluents tions (Sun & Zhou 2016). rates after 30 days were between 37.2 and (Khandare et al. 2011). In another study on For the treatment of PHCs-contaminated 49.4%, (control only 12.9%). Removal rates phytoremediation of dyes from textile soil, Iris dichotoma and I. lactea were inves- of TPH composition were also significantly wastewater, Tagetes patula, Aster amellus, tigated in a pot culture experiment. These higher than controls, and Fourier trans- Portulaca grandiflora and Gaillardia grandi- species were found to promote degrada- form infrared spectroscopy confirmed the flora were tested separately, finding that tion of fractions of PHCs. I. lactea tolerated presence of oil in the plant tissues (Liu et within 30 days they reduced the color high concentration of PHCs (40,000 mg al. 2012). value by 59, 50, 46 and 73%, respectively. kg-1) and showed a good degradation rate Plants of Portulaca oleracea were able to Only a minor decrease in plant growth was of petroleum hydrocarbons. In contrast, I. remove fluoride from a 10 mg L-1 NaF solu- iForest 13: 139-151 145 Capuana M - iForest 13: 139-151 y

r tion, within 15 days by 73%; the higher fluo- PAHs (Wei & Pan 2010). (Becerra-Castro et al. 2013). t

s ride concentrations showed lower removal Concerning polychlorinated biphenyls Many studies assess the remediation of e

r rates (Khandare et al. 2017). Canna indica (PCB), Terzaghi et al. (2019) demonstrated metal-polluted soil with the help of several o was studied in a hydroponic system for that Festuca arundinacea cultivated by agents, mainly synthetic organic chelates, F testing its ability to remediate triazophos adding compost or in consociation with Cu- but also natural organic compounds and in- d n contamination, a harmful pesticide. After curbita pepo ssp. pepo and Medicago sativa organic products, that overcome limita- a 21 days of exposure, a significant percent- cultivated with Rhizobium spp. and mycor- tions to phytoremediation due to low met- s e age of the substance was removed from rhizal fungi reduced total PCB concentra- al solubility and availability (Leštan et al. c

n the substrate (Cheng et al. 2007). Among tions by about 20%, with a significant deple- 2008). Nevertheless, the high cost of these e i numerous other cases, Chrysanthemum tion in a high number of PCB congeners. In products and the possible toxic outflow c

s morifolium can simultaneously absorb and an in vitro experiment, Petunia grandiflora into the environment have to be taken into o purify benzene and formaldehyde to a and Gaillardia grandiflora, when cultured account. Below, a few cases are mentioned e g large extent, while Aloe vera var. chinensis together, showed a great effectiveness in as examples. o i can absorb formaldehyde; Crassula portu- degrading and removing a dye mixture The application to soil of sodium dodecyl B lacea is active towards benzene, and Di- from the substrate in 36 h, with results sig- sulfate (SDS), ethylenediaminetriacetic – anthus chinensis towards sulfur dioxide (Liu nificantly higher than those detected from acid (EDTA) and ethylenegluatarotriacetic t s et al. 2007). the cultivars in isolation (Watharkar & Jad- acid (EGTA) to enhance Cd remediation e r Wild ornamentals with high ornamental hav 2014). was studied with Calendula officinalis. EDTA o

F value, fast growth and extensive root sys- was observed to be toxic to the plants, i tems are, in general, a suitable solution, Enhanced phytoremediation while the addition of SDS and/or EGTA re- when deemed capable of degrading con- It is worth noting that, for several tree sulted in significantly increased plant bio- taminants, due to their broad adaptability, species, the plant-fungi-bacterium system mass (p < 0.05). Almost all of the treat- widespread distribution and ease of culti- represents an important interactive bal- ments containing SDS or/and EGTA led to vation (Cheng & Zhou 2014). ance for the implementation of the phy- an increase in the total Cd content in the toremediation activity, as recently ob- plants (Liu et al. 2010). For enhancing the Consociations served in hybrid poplar (Populus deltoides × uptake and translocation of Cd, Cr, and Ni, Soils are often polluted by different met- P. nigra) and willow (Salix purpurea subsp. two cultivars of Helianthus annuus were als or organic compounds, so phytoremedi- lambertiana – Guarino et al. 2018). Eucalyp- used in conjunction with EDTA and citric ation may require multiple plant species tus camaldulensis also demonstrated in- acid (CA) as chelators. EDTA at a concen- and ecotypes since most of the plants creased effectiveness in extraction, up- tration of 0.1 g kg-1 produced the best re- suited to this purpose show an aptitude to take, and translocation of Cd when inocu- sults for both cultivars, while the highest accumulate only one or a few pollutants. lated with arbuscular mycorrhiza fungi or CA concentrations had a phytotoxic effect A pot experiment was carried out with plant growth promoting rhizobacteria (Mo- (Turgut et al. 2004). In Althaea rosea, EDTA the aim of determining the phytoextrac- tesharezadeh et al. 2017). As an example and tannic acid led to higher heavy metal tion potential of the hyperaccumulator for herbaceous species, Helianthus annuus removal of Cd, Ni, Pb and Cu from an artifi- Pteris vittata when co-planted with a inoculated with Bacillus safensis and/or Ko- cially contaminated soil, with significant woody tree (Morus alba or Broussonetia pa- curia rosea was tested in soil with four lev- heavy metal accumulation in stems and pyrifera) in soil contaminated with Cd, Pb, els of Ni concentrations (0, 150, 300, and leaves (Cay et al. 2015). Zn, or As. The uptake of As was signifi- 450 mg kg-1), finding that the highest Ni up- In view of a more environmentally friend- cantly increased when co-planted with take was observed at Ni 300, when the ly choice, less harmful products can be Morus or Broussonetia (by 80.0% and 64.2% sunflower seed was co-inoculated by B. used. Amaranthus caudatus showed an in- respectively). However, co-plantation did safensis + K. rosea (Mohammadzadeh et al. creased capacity to uptake cadmium when not have a promoting effect on the metal 2014). solutions of tea saponin (extracted from accumulation of both M. alba L. and B. pa- With regard to organic pollutants, endo- camellia seeds) or EDTA were supplied to pyrifera (Zeng et al. 2019). phyte-assisted phytoremediation of a site the soil, detecting TF >1, with better values In the case a huge expanse of land, a contaminated with Trichloroethylene (TCE) for saponin (Cay 2016). In a pot experiment consociation of grasses could be a good so- was studied using Populus deltoides × nigra with Helianthus annuus, the effects of cul- lution. Work by Maila et al. (2005) demon- inoculated with a strain of Enterobacter. ture in a soil contaminated with Cd and Zn strated the potential of the grass species The inoculated trees showed an increased and amended with swine manure, salicylic Brachiaria serrata and Eleusine corocana in growth and a reduced toxic effect com- acid (SA), or potassium chloride (KCl) decontaminating PAHs-contaminated soil. pared to control, excreting 50% more chlo- were assessed. The three amendments in- It was found that after a ten-week treat- ride ions into the rhizosphere, a good sig- creased sunflower biomass, height, and ment the naphthalene concentration was nal of an increased TCE metabolism in plan- flower diameter. Manure significantly de- undetectable in the “multispecies” vege- ta. A significant decrease in the concentra- creased the bioaccumulation coefficient tated soil compared to 96% removal effi- tion of TCE and its derivatives from the (BCF) of Cd and Zn, while KCl increased the ciency in the monoplanted treatment and tree-associated groundwater plume was BCF of Cd. Either swine manure and KCl in- 63% in the control. For the same contami- also detected (Doty et al. 2017). With hy- creased Cd and Zn translocation from roots nants, ryegrass (Lolium perenne), white brid poplar clones associated to Arthrobac- to aboveground parts, while swine manure clover (Trifolium repens) and celery (Apium ter strains, the possibility to rhizoremedi- and SA reduced the Cd/Zn ratios in flowers graveolens) were tested, finding that the ate soils contaminated with the insecticide (Hao et al. 2012). remaining percentage of PAHs in mixtures exachlorocyclohexane (HCH) isomers was Within this wide frame, the development was significantly lower than those in mono- demonstrated, stressing the importance of of transgenic plants with enhanced phy- cultures and non-planted soils (Meng et al. in situ pre-selection of the best candidate toremediation capacity is also a possible 2011). Another work proved that Brassica plants and bacteria strains (Bianconi et al. approach (Shah & Pathak 2019), but the campestris showed low removal of PAHs, 2011). The shrub Cytisus striatus, also in as- general opposition of public opinion to the while Medicago sativa had the highest po- sociation with microbial inoculants (Rhodo- introduction of genetically modified plant tential for remediation of phenanthrene coccus erythropolis and Sphingomonas sp.) species has to be carefully considered. and Trifolium repens for pyrene; but mixed showed an interesting activity on the dissi- cropping (rape with white clover or alfalfa, pation of the HCH. HCH concentration in Conclusions Medicago sativa) showed far better results soil was reduced after plant growth and, The use of ornamental (woody and flow- than single cropping for the remediation of more significantly, with inoculated plants ering) plants for the phytoremediation of

146 iForest 13: 139-151 Phytoremediation in urban areas y

urban and periurban environments shows Acknowledgements New York, USA, pp. 53-70. r t

many positive aspects that have been high- I gratefully acknowledge Mrs. Catia Boggi Boll T, Von Haaren C, Albert C (2014). How do ur- s

ban dwellers react to potential landscape e lighted in this work. The “multipurpose” and Mr. Gabriele Cencetti for their cooper- r function of these plants plays an important ation in the information retrieval and for changes in recreation areas? A case study with o F role in the environmental restoration and the images provided. The manuscript was particular focus on the introduction of dendro- d aesthetic enhancement, but the success of greatly improved by the comments pro- mass in the Hamburg Metropolitan Region. n a the phytoremediation strategy lies in the vided by two anonymous reviewers. iForest - Biogeoscience and Forestry 7 (6): 423- s careful choice of species and/or genotypes 433. - doi: 10.3832/ifor1173-007 e c

matching the specific environments and References Borghi M, Tognetti R, Monteforti G, Sebastiani L n e pollutants. Abbasi H, Pourmajidian MR, Hodjati SM, Fallah A, (2007). Responses of Populus × euramericana i c

From the review of the available litera- Nath S (2017). Effect of soil-applied lead on (P. deltoides × P. nigra) clone Adda to increasing s ture it emerged that, trees in general, even mineral contents and biomass in Acer cappado- copper concentrations. Environmental and Ex- o e if not classifiable as hyperaccumulators, cicum, Fraxinus excelsior and Platycladus orien- perimental Botany 61: 66-73. - doi: 10.1016/j.env g o display a greater potential for exploitation talis seedlings. iForest - Biogeoscience and For- expbot.2007.03.001 i B in phytoremediation compared to herba- estry 10 (4): 722-728. - doi: 10.3832/ifor2251-010 Bosiacki M (2008). Accumulation of cadmium in – ceous species. This is simply due to the Abrahams PW (2002). Soils: their implications to selected species of ornamental plants. Acta Sci- t greater biomass growth potential and human health. Science of the Total Environ- entiarium Polonorum Hortorum Cultus 7 (2): 21- s e rooting system depth of woody species. ment 291: 1-32. - doi: 10.1016/S0048-9697(01)011 31. r o

On the other hand, herbaceous species are 02-0 Bosiacki M, Wojciechowska E (2012). Phytoex- F i characterised by higher variability and plas- Adhikari T, Kumar A (2012). Phytoaccumulation traction of nickel by selected ornamental ticity, and offer the possibility of frequent and tolerance of Ricinus communis L. to nickel. plants. Ecological Chemistry and Engineering 19 replacements. International Journal of Phytoremediation 14: (3): 331-345. - doi: 10.2478/v10216-011-0024-9 Among trees, Salicaceae are probably the 481-492. - doi: 10.1080/15226514.2011.604688 Bretzel F, Calderisi M (2006). Metal contamina- most investigated species for phytoremedi- Aitchison EW, Kelley SL, Alvarez PJJ, Schoor JL tion in urban soils of coastal Tuscany (Italy). En- ation purposes (Marmiroli et al. 2011). (2000). Phytoremediation of 1,4-dioxane by hy- vironmental Monitoring and Assessment 118: Great interest is addressed to Salix spp., brid poplar trees. Water Environment Research 319-335. - doi: 10.1007/s10661-006-1495-5 while poplars are now considered to be 72: 313-321. - doi: 10.2175/106143000X137536 Budak F, Zaimoglu Z, Basci N (2011). Uptake and model species, comparable to Arabidopsis Amari T, Ghnaya T, Sghaier S, Porrini M, Lucchini translocation of hexavalent chromium by se- among herbaceous plants. Due to their G, Sacchi AG, Abdelly C (2016). Evaluation of lected species of ornamental plants. Polish adaptability to different environments, fast Ni2+ phytoextraction potential in Mesembryan- Journal of Environmental Studies 20: 857-862. growth, ease of propagation and good per- themum crystallinum (halophyte) and Brassica [online] URL: http://www.researchgate.net/pu formances when exposed to some pollu- juncea. Journal of Bioremediation and Biodeg- blication/288111790 tants, these species might possess some radation 7 (2): 336. - doi: 10.4172/2155-6199.1000 Burken JG, Schnoor JL (1997). Uptake and me- useful practical applications in phytoreme- 336 tabolism of atrazine by poplar trees. Environ- diation, particularly in peri-urban areas. For Baz M, Fernandez RT (2002). Evaluating woody mental Science and Technology 31: 1399-1406. - urban environments, several other woody ornamentals for use in herbicide phytoremedia- doi: 10.1021/es960629v species are probably more suitable, being tion. Journal of the American Society for Horti- Cachada A, Pato P, Rocha-Santos T, Ferreira Da characterised by a higher ornamental val- cultural Science 127 (6): 991-997. - doi: 10.21273/ Silva E, Duarte AC (2012). Levels, sources and ue. Among flowering herbaceous plants, JASHS.127.6.991 potential human health risks of organic pollu- the possibility of choice is significantly Becerra-Castro C, Kidd PS, Rodríguez-Garrido B, tants in urban soils. Science of Total Environ- wider; for instance, the Asteraceae family Monterroso C, Santos-Ucha P, Prieto-Fernán- ment 430: 184-192. - doi: 10.1016/j.scitotenv.20 shows a wide range of interesting species dez A (2013). Phytoremediation of hexachloro- 12.04.075 (Nikolić & Stevović 2015) with sunflowers cyclohexane (HCH)-contaminated soils using Cai Z, Zhou QX, Peng SW, Li KN (2010). Promoted having been studied in depth and demon- Cytisus striatus and bacterial inoculants in soils biodegradation and microbiological effects of strating a high capacity to remediate spe- with distinct organic matter content. Environ- petroleum hydrocarbons by Impatiens balsam- cific pollutants. mental Pollution 178: 202-210. - doi: 10.1016/j.en ina L. with strong endurance. Journal of Haz- Several interesting species are yet to be vpol.2013.03.027 ardous Material 183: 731-737. - doi: 10.1016/j.jhaz explored, and special attention should be Berndes G, Fredrikson F, Borjesson P (2004). mat.2010.07.087 paid to the huge possibilities offered by Cadmium accumulation and Salix-based phy- Caldelas JL, Araus A, Febrero J (2012). Accumula- plant consociation, including aspects re- toextraction on arable land in Sweden. Agricul- tion and toxic effects of chromium and zinc in lated to modifications in the structure of ture, Ecosystem and Environment 103: 207-223. Iris pseudacorus L. Acta Physiologiae Plantarum the rhizosphera. Within this topic, possible - doi: 10.1016/j.agee.2003.09.013 34: 1217-1228. - doi: 10.1007/s11738-012-0956 associations between herbaceous plants, Bianconi D, De Paolis MR, Agnello AC, Lippi D, Carrus G, Scopelliti M, Lafortezza R, Colangelo G, trees or between herbaceous and woody Pietrini F, Zacchini M, Polcaro C, Donati E, Paris Ferrini F, Salbitano F, Agrimi M, Portoghesi L, plants are practically infinite, allowing a P, Spina S, Massacci A (2011). Field-scale rhy- Semenzato P, Sanesi G (2015). Go greener, feel perfect adhesion to the needs of each spe- zoremediation of a contaminated soil with hex- better? The positive effects of biodiversity on cific environment, and making phytoreme- achlorocyclohexane (HCH) isomers: the poten- the well-being of individuals visiting urban and diation an “aesthetic experience”, as pro- tial of poplars for environmental restoration peri-urban green areas. Landscape and Urban posed by Sleegers (2010). and economical sustainability. In: “Handbook Planning 134: 221-228. - doi: 10.1016/j.landurb Finally, efforts are required to overcome of Phytoremediation” (Golubev IA ed). Nova plan.2014.10.022 problems related to the disposal of con- Science Publishers, Inc, New York, USA, pp. Cay S (2016). Enhancement of cadmium uptake taminated materials and how to limit the 783-794. by Amaranthus caudatus, an ornamental plant, costs related to the exploitation of this Biasioli M, Barberis R, Ajmone-Marsan F (2006). using tea saponin. Environmental Monitoring technique. The influence of a large city on some soil prop- and Assessment 188: 1-8. - doi: 10.1007/s10661- In synthesis, phytoremediation could now erties and metals content Science of the Total 016-5334-z be seen as part of a multifunctional proc- Environment 356: 154-164. - doi: 10.1016/j.scitot Cay S, Uyanik A, Engin MS, Kutbay HG (2015). Ef- ess that creates a green infrastructure net- env.2005.04.033 fect of EDTA and tannic acid on the removal of work defining evolving landscapes, not Blaylock MJ, Huang JW (2000). Phytoextraction Cd, Ni, Pb and Cu from artificially contaminated only in the countryside but also in urban of metals. In: “Phytoremediation of Toxic Met- soil by Althaea rosea Cavan. International Jour- environments. als: Using Plants to Clean up the Environment” nal of Phytoremediation 17 (1-6): 568-574. - doi: (Raskin I, Ensley BD eds). John Wiley and Sons, 10.1080/15226514.2014.935285 iForest 13: 139-151 147 Capuana M - iForest 13: 139-151 y

r Chandanshive VV, Kadam SK, Khandare RV, Ku- 66: 505-513. - doi: 10.1016/j.chemosphere.2006. phytoextraction of HMs at real scale, by com- t

s rade MB, Jeon BH, Jadhav JP, Govindwar SP 05.065 bining Salicaceae trees with microbial consor- e (2018). In situ phytoremediation of dyes from Di Baccio D, Tognetti R, Sebastiani L, Vitagliano C tia. Frontiers in Environmental Science 6: 137. - r o textile wastewater using garden ornamental (2003). Responses of Populus deltoids × P. nigra doi: 10.3389/fenvs.2018.00137 F plants, effect on soil quality and plant growth. (P. × euramericana) clone I-214 to high zinc con- Guerra F, Gainza F, Pérez R, Zamudio F (2011). d

n Chemosphere 210: 968-976. - doi: 10.1016/j.che centrations. New Phytologist 159: 443-452. - Phytoremediation of heavy metals using pop- a mosphere.2018.07.064 doi: 10.1046/j.1469-8137.2003.00818.x lars (Populus spp.): a glimpse of the plant re- s e Chen B, Adimo OA, Bao Z (2009). Assessment of Doty SL, Freeman JL, Cohu CM, Burken JG, Firrin- sponses to copper, cadmium and zinc stress. c

n aesthetic quality and multiple functions of ur- cieli A, Simon A (2017). Enhanced degradation In: “Handbook of Phytoremediation” (Golubev e i ban green space from the users’ perspective: of TCE on a superfund site using endophyte-as- IA ed), Nova Science Publishers, Inc, New York, c

s the case of Hangzhou Flower Garden, China. sisted poplar tree phytoremediation. Environ- USA, pp. 387-413. o Landscape and Urban Planning 93 (1): 76-82. - mental Science and Technology 51 (17): 10050- Guidi W, Kadri H, Labrecque M (2012). Establish- e

g doi: 10.1016/j.landurbplan.2009.06.001 10058. - doi: 10.1021/acs.est.7b01504 ment techniques to using willow for phytore- o i Cheng L, Wang Y, Cai Z, Liu J, Yu B, Zhou Q Ehsan N, Nawaz R, Ahmad S, Khan MM, Hayat J mediation on a former oil refinery in southern B

(2017). Phytoremediation of petroleum hydro- (2016a). Phytoremediation of chromium-con- Quebec: achievements and constraints. Chem- – carbon-contaminated saline-alkali soil by wild taminated soil by an ornamental plant, vinca istry and Ecology 28 (1): 49-64. - doi: 10.1080/ t s ornamental Iridaceae species. International (Vinca rosea L.). Journal of Environmental and 02757540.2011.627857 e r Journal of Phytoremediation 19 (3): 300-308. - Agricultural Sciences 7: 29-34. [online] URL: Guidi W, Pitre FE, Labrecque M (2013). Short-ro- o

F doi: 10.1080/15226514.2016.1225282 http://www.agropublishers.com/files/JEAS75.P tation coppice of willows for the production of i Cheng LJ, Zhou QX (2014). Phytoremediation of DF biomass in Eastern Canada. In: “Biomass Now petroleum hydrocarbon contaminated soils us- Ehsan N, Nawaz R, Ahmad S, Arshad M, Umair Sustainable Growth and Use” (Matovic MD ed), ing a wild ornamental plant Hylotelephium M, Mahmood R (2016b). Use of ornamental InTech Open Science, pp. 421-448. - doi: 10.5772/ spectabile (Boreau) H. Ohba. Acta Scientiae Cir- plant “Vinca” (Vinca rosea L.) for remediation 51111 cumstantiae 34: 980-986. of lead-contaminated soil. Journal of Biodiver- Guidi Nissim W, Pitre FE, Kadri H, Desjardins D, Cheng S, Xiao J, Xiao H, Zhang L, Wu Z (2007). sity and Environmental Sciences 8 (3): 46-54. Labrecque M (2014a). Early response of willow Phytoremediation of triazophos by Canna in- [online] URL: http://www.researchgate.net/pu to increasing silver concentration exposure. In- dica Linn. in a hydroponic system. International blication/299229602 ternational Journal of Phytoremediation 16: Journal of Phytoremediation 9: 453-463. - doi: Ehsan N, Nawaz R, Ahmad S, Arshad M, Umair 660-670. - doi: 10.1080/15226514.2013.856840 10.1080/15226510701709531 M, Sarmad M (2016c). Remediation of heavy Guidi Nissim W, Voicu A, Labrecque M (2014b). Chiesura A (2004). The role of urban parks for metal-contaminated soil by ornamental plant Willow short-rotation coppice for treatment of the sustainable city. Landscape and Urban Plan- zinnia (Zinnia elegance L.). Asian Journal of polluted groundwater. Ecological Engineering ning 68: 129-138. - doi: 10.1016/j.landurbplan.20 Chemistry 28 (6): 1338-1342. - doi: 10.14233/aj 62: 102-114. - doi: 10.1016/j.ecoleng.2013.10.005 03.08.003 chem.2016.19701 Gülser F, Cig A, Sönmez F (2011). The determina- Chintakovid P, Visoottiviseth S, Khokiattiwong S Facciotto G, Minotta G, Paris P, Pelleri F (2014). tion of phytoremediation levels of ornamental (2008). Potential of the hybrid marigolds for ar- Tree farming, agroforestry and the new green plants used in landscape. Journal of Interna- senic phytoremediation and income generation revolution. A necessary alliance. In: Proceed- tional Environmental Application and Science 6: of remediators in Ron Phibun District, Thailand. ings of the “Second International Congress of 661-667. [online] URL: http://dergipark.org.tr/ Chemosphere 70: 1532-1537. - doi: 10.1016/j.che Silviculture”. Florence (Italy) 26-29 Nov 2014, download/issue-full-file/16181 mosphere.2007.08.031 pp. 7. [online] URL: http://www.researchgate. Han Y, Yuan H, Huang S, Guo Z, Xia B, Gu J Compernolle T, Van Passel S, Weyens N, Van- net/publication/291153366 (2007). Cadmium tolerance and accumulation gronsveld J, Lebbe L, Thewys T (2012). Ground- Ferrini F, Fini A (2011). Sustainable management by two species of Iris. Ecotoxicology 16: 557- water remediation and the cost effectiveness techniques for trees in the urban areas. Journal 563. - doi: 10.1007/s10646-007-0162-0 of phytoremediation. International Journal of of Biodiversity and Ecological Sciences 1: 1-19. Hao XZ, Zhou DM, Li DD, Jiang P (2012). Growth, Phytoremediation 14 (9): 861-877. - doi: 10.1080/ [online] URL: http://www.sid.ir/en/journal/View cadmium and zinc accumulation of ornamental 15226514.2011.628879 Paper.aspx?ID=202617 sunflower (Helianthus annuus L.) in contami- Conway TM, Vander Vecht J (2015). Growing a di- Forte J, Mutiti S (2017). Phytoremediation poten- nated soil with different amendments. Pedo- verse urban forest: species selection decisions tial of Helianthus annuus and Hydrangea panicu- sphere 22: 631-639. - doi: 10.1016/S1002-0160(12) by practitioners planting and supplying trees. lata in copper and lead-contaminated soil. Wa- 60048-4 Landscape and Urban Planning 138: 1-10. - doi: ter, Air and Soil Pollution 228: 77. - doi: 10.1007/ Henry HF, Burken JG, Maier RM, Newman LA, 10.1016/j.landurbplan.2015.01.007 s11270-017-3249-0 Rock S, Schnoor JL, Suk WA (2013). Phytotech- Cunningham SD, Berti WR (1993). Remediation Garbisu C, Alkorta I (2001). Phytoextraction: A nologies: preventing exposures, improving of contaminated soils with green plants: an cost-effective plant-based technology for the public health. International Journal of Phytore- overview. In Vitro Cellular and Developmental removal of metals from the environment. mediation 15: 889-899. - doi: 10.1080/15226514. Biology - Plant 29: 207-212. - doi: 10.1007/BF0263 Bioresource Technology 77 (3): 229-236. - doi: 2012.760521 2036 10.1016/S0960-8524(00)00108-5 Houda Z, Bejaou Z, Albouchi A, Gupta DK, Corpas Dadea C, Russo A, Tagliavini M, Mimmo T, Zerbe Garcia R, Millan E (1998). Assessment of Cd, Pb, FJ (2016). Comparative study of plant growth S (2017). Tree species as tools for biomonitor- and Zn contamination in roadside soils and of two poplar tree species irrigated with ing and phytoremediation in urban environ- grasses from Gipuzkoa (Spain). Chemosphere treated wastewater, with particular reference ments: a review with special regard to heavy 37 (8): 1615-1625. - doi: 10.1016/S0045-6535(98) to accumulation of heavy metals (Cd, Pb, As, metals. Arboriculture and Urban Forestry 43: 00152-0 and Ni). Environmental Monitoring and Assess- 155-167. Giachetti G, Sebastiani L (2006). Development ment 188: 99. - doi: 10.1007/s10661-016-5102-0 Desjardins D, Pitre FE, Guidi Nissim W, Labrecque and chromium uptake in hybrid poplars culti- Huang H, Yu N, Wang L, Gupta D, He Z, Wang K, M (2016). Differential uptake of silver, copper vated on substrate polluted with industrial Zhu Z, Yan X, Li T, Yang Xe (2011). The phytore- and zinc suggests complementary species-spe- slags. Advances in Horticultural Science 20: 193- mediation potential of bioenergy crop Ricinus cific phytoextraction potential. International 198. communis for DDTs and cadmium co-contami- Journal of Phytoremediation 18: 598-604. - doi: Goswami S, Das S (2016). Copper phytoremedia- nated soil. Bioresource Technology 102 (23): 10.1080/15226514.2015.1086296 tion potential of Calendula officinalis L. and the 11034-11038. - doi: 10.1016/j.biortech.2011.09.067 De Miguel E, Iribarren I, Chacon E, Ordonez A, role of antioxidant enzymes in metal tolerance. Huinink JTM (1998). Soil quality requirements for Charlesworth S (2006). Risk-based evaluation Ecotoxicology and Environmental Safety 126: use in urban environments. Soil and Tillage Re- of the exposure of children to trace elements 211-218. - doi: 10.1016/j.ecoenv.2015.12.030 search 47 (1-2): 157-162. - doi: 10.1016/S0167-1987 in playgrounds in Madrid (Spain). Chemosphere Guarino C, Paura B, Sciarrillo R (2018). Enhancing (98)00087-7

148 iForest 13: 139-151 Phytoremediation in urban areas y

Huq SMI, Joardar JC, Parvin S (2005). Marigold of applying ornamental plants in contaminated Current Opinion in Biotechnology 14: 277-282. - r t

(Tagetes patula) and ornamental arum (Syngo- soil remediation. Chinese Journal of Applied doi: 10.1016/S0958-1669(03)00060-0 s

nia sp.) as phytoremediators for arsenic in pot Ecology 18: 1617-1623. Meers E, Vandecasteele B, Ruttens A, Vangrons- e r

soil. Bangladesh Journal of Botany 34 (2): 65- Liu J, Schnoor JL (2008). Uptake and transloca- veld J, Tack FMG (2007). Potential of five wil- o F 70. tion of lesser-chlorinated polychlorinated bi- low species (Salix spp.) for phytoextraction of d

Hussain S, Akram M, Abbas G, Murtaza B, Shahid phenyls (PCBs) in whole hybrid poplar plants heavy metals. Environmental and Experimental n a M, Shah NS, Bibi I, Niazi NK (2017). Arsenic tol- after hydroponic exposure. Chemosphere 73: Botany 60 (1): 57-68. - doi: 10.1016/j.envexpbot. s

erance and phytoremediation potential of Co- 1608-1616. - doi: 10.1016/j.chemosphere.2008.0 2006.06.008 e c

nocarpus erectus L. and Populus deltoides L. In- 8.009 Meng L, Qiao M, Arp H (2011). Phytoremediation n e

ternational Journal of Phytoremediation 19 (11): Liu J, Zhou QX, Sun T, Ma LQ, Wang S (2008). efficiency of a PAH-contaminated industrial soil i c

985-991. - doi: 10.1080/15226514.2017.1303815 Growth responses of three ornamental plants using ryegrass, white clover, and celery as s

Jensen JK, Holm PE, Nejrup J, Larsen MB, Borg- to Cd and Cd-Pb stress and their metal accumu- mono- and mixed cultures. Journal of Soils and o e

gaard OK (2009). The potential of willow for relation characteristics. Journal of Hazardous Ma- Sediments 11 (3): 482-490. - doi: 10.1007/s11368- g o

mediation of heavy metal polluted calcareous terials 151 (1): 261-267. - doi: 10.1016/j.jhazmat. 010-0319-y i B

urban soils. Environmental Pollution 157: 931-37. 2007.08.016 Miao Q, Yan JH (2013). Comparison of three or- – - doi: 10.1016/j.envpol.2008.10.024 Liu Z, He XY, Chen W, Yuan FH, Yan K, Tao DL namental plants for phytoextraction potential t

Khalid S, Shahid M, Niazi NK, Murtaza B, Bibi I, (2009). Accumulation and tolerance character- of chromium removal from tannery sludge. s e

Dumat C (2017). A comparison of technologies istics of cadmium in a potential hyperaccumula- Journal of Material Cycles and Waste Manage- r o

for remediation of heavy metal contaminated tor - Lonicera japonica Thunb. Journal of Haz- ment 15 (1): 98-105. - doi: 10.1007/s10163-012- F i soils. Journal of Geochemical Exploration 182: ardous Materials 169 (1-3): 170-175. - doi: 0095-4 247-268. - doi: 10.1016/j.gexplo.2016.11.021 10.1016/j.jhazmat.2009.03.090 Miller RW, Hauer RJ, Werner LP (2015). Urban Khandare RV, Desai SB, Bhujbal SS, Watharkar Liu J, Zhou Q, Wang S (2010). Evaluation of forestry: planning and managing urban green- AD, Biradar SP, Pawar PK, Govindwar SP (2017). chemical enhancement on phytoremediation spaces (3rd edn). Waveland Press, Long Grove, Phytoremediation of fluoride with garden orna- effect of Cd-contaminated soils with Calendula IL, USA, pp. 560. [online] URL: http://books. mentals Nerium oleander, Portulaca oleracea, officinalis L. International Journal of Phytore- google.com/books?id=VdI_CQAAQBAJ and Pogonatherum crinitum. Environmental Sci- mediation 12 (5): 503-515. - doi: 10.1080/1522651 Mleczek M, Rutkowski P, Rissmann I, Kaczmarek ence and Pollution Research 24 (7): 6833-6839. 0903353112 Z, Golinski P, Szentner K, Strazynska K, Sta- - doi: 10.1007/s11356-017-8424-8 Liu R, Jadeja RN, Zhou Q, Liu Z (2012). Treatment chowiak A (2010). Biomass productivity and Khandare NOR, Kabra A, Tamboli D, Govindwar S and remediation of petroleum-contaminated phytoremediation potential of Salix alba and (2011). The role of Aster amellus Linn. in the soils using selective ornamental plants. Envi- Salix viminalis. Biomass and Bioenergy 34 (9): degradation of a sulfonated azo dye Remazol ronmental Engineering Science 29 (6): 494-501. 1410-1418. - doi: 10.1016/j.biombioe.2010.04.012 Red: a phytoremediation strategy. Chemo- - doi: 10.1089/ees.2010.0490 Mohammadzadeh A, Tavakoli M, Chaichi MR, sphere 82 (8): 1147-1154. - doi: 10.1016/j.chemo Liu J, Xin X, Zhou Q (2018). Phytoremediation of Motesharezadeh B (2014). Effects of nickel and sphere.2010.12.073 contaminated soils using ornamental plants. PGPBs on growth indices and phytoremedia- Killi D, Bussotti F, Gottardini E, Pollastrini M, Environmental Reviews 26 (1): 43-54. - doi: tion capability of sunflower (Helianthus annuus Mori J, Tani C (2018). Photosynthetic and mor- 10.1139/er-2017-0022 L.). Archives of Agronomy and Soil Science 60 phological responses of oak species to temper- Livesley SJ, McPherson GM, Calfapietra C (2016). (12): 1765-1778. - doi: 10.1080/03650340.2014.89

ature and [CO2] increased to levels predicted The urban forest and ecosystem services: im- 8839 for 2050. Urban Forestry and Urban Greening pacts on urban water, heat, and pollution cy- Motesharezadeh B, Kamalpoor S, Alikhani HA, 31: 26-37. - doi: 10.1016/j.ufug.2018.01.012 cles at the tree, street, and city Scale. Journal Zarei M, Azimi S (2017). Investigating the ef- Landberg T, Greger M (1994). Can heavy metal of Environmental Quality 45: 119-124. - doi: fects of plant growth promoting bacteria and tolerant clones of Salix be used as vegetation 10.2134/jeq2015.11.0567 Glomus mosseae on cadmium phytoremedia- filters on heavy metal contaminated land? In: Ljung K, Selinus O, Otabbong E (2006a). Metals tion by Eucalyptus camaldulensis L. Pollution 3: “Willow Vegetation Filters for Municipal Waste- in soils of children’s urban environments in the 575-588. - doi: 10.22059/poll.2017.62774 waters and Sludges. A Biological Purification small northern European city of Uppsala. Sci- Mukherjee A, Agrawal M (2018). Use of GLM ap- System” (Aronsson P, Perttu K eds). Swedish ence of the Total Environment 366 (2-3): 749- proach to assess the responses of tropical University of Agricultural Sciences, Uppsala, 759. - doi: 10.1016/j.scitotenv.2005.09.073 trees to urban air pollution in relation to leaf pp. 133-144. [online] URL: https://inis.iaea.org Ljung K, Selinus O, Otabbong E, Berglund M functional traits and tree characteristics. Eco- /collection/NCLCollectionStore/_Public/27/044/2 (2006b). Metal and arsenic distribution in soil toxicology and Environmental Safety 152: 42- 7044436.pdf#page=123 particle sizes relevant to soil ingestion by chil- 54. - doi: 10.1016/j.ecoenv.2018.01.038 Lee S-C, Li X, Shi W, Cheung S-C, Thornton I dren. Applied Geochemistry 21 (9): 1613-1624. - Nanda Kumar PBA, Dushenkov V, Motto H, Ras- (2006). Metal contamination in urban, subur- doi: 10.1016/j.apgeochem.2006.05.005 kin I (1995). Phytoextraction: the use of plants ban, and country park soils of Hong Kong: a Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, to remove heavy metals from soils. Environ- study based on GIS and multivariate statistics. Wang Q, Li R, Zhang Z (2016). Challenges and mental Science and Technology 29 (5): 1232- Science of the Total Environment 356 (1-3): 45- opportunities in the phytoremediation of heavy 1238. - doi: 10.1021/es00005a014 61. - doi: 10.1016/j.scitotenv.2005.03.024 metals contaminated soils: a review. Ecotoxi- Nikolić M, Stevović S (2015). Family Asteraceae Leštan D, Luo C-I, Li X- (2008). The use of chelat- cology and Environmental Safety 126: 111-121. - as a sustainable planning tool in phytoremedia- ing agents in the remediation of metal-contam- doi: 10.1016/j.ecoenv.2015.12.023 tion and its relevance in urban areas. Urban inated soils: a review. Environmental Pollution Maila M, Randima P, Cloete TE (2005). Multispe- Forestry and Urban Greening 14: 782-789. - doi: 153: 3-13. - doi: 10.1016/j.envpol.2007.11.015 cies and monoculture rhizoremediation of poly- 10.1016/j.ufug.2015.08.002 Lewandowski I, Schmidt U, Londo M, Faaij A cyclic aromatic hydrocarbons (PAHs) from the Pajević S, Borišev M, Nikolić N, Arsenov D, Orlov- (2006). The economic value of the phytoreme- soil. International Journal of Phytoremediation ić S, Zupunski M (2016). Phytoextraction of diation function - assessed by the example of 7 (2): 87-98. - doi: 10.1080/16226510590950397 heavy metals by fast-growing trees: a review. cadmium remediation by willow (Salix ssp.). Marmiroli M, Pietrini F, Maestri E, Zacchini M, In: “Phytoremediation Management of Envi- Agricultural Systems 89 (1): 68-89. - doi: 10.101 Marmiroli N, Massacci A (2011). Growth, physio- ronmental Contaminants” (Ansari AA, Gill SS, 6/j.agsy.2005.08.004 logical and molecular traits in Salicaceae trees Gill R, Lanza GR, Newman L eds). Springer In- Li XX, Zhou ZK (2005). Endemic wild ornamental investigated for phytoremediation of heavy ternational Publishing, Cham, Switzerland, pp. plants from Northwestern Yunnan, China. Hort- metals and organics. Tree Physiology 31: 1319- 29-64. - doi: 10.1007/978-3-319-40148-5_2 science 40: 1612-1619. - doi: 10.21273/HORTSCI. 1334. - doi: 10.1093/treephys/tpr090 Pathak V, Tripathi BD, Mishra VK (2011). Evalua- 40.6.1612 McGrath SP, Zhao FJ (2003). Phytoextraction of tion of anticipated performance index of some Liu J, Zhou QX, Sun T, Wang XF (2007). Feasibility metals and metalloids from contaminated soils. tree species for green belt development to mit- iForest 13: 139-151 149 Capuana M - iForest 13: 139-151 y

r igate traffic generated noise. Urban Forestry ban tree cadastre data. Sustainability 10 (3): 1- Terzaghi E, Vergani L, Mapelli F, Borin S (2019). t

s and Urban Greening 10 (1): 61-66. - doi: 18. - doi: 10.3390/su10020001 Rhizoremediation of weathered PCBs in a heav- e 10.1016/j. ufug.2010.06.008 Shah K, Pathak L (2019). Transgenic energy ily contaminated agricultural soil: results of a r o Pulford ID, Watson C (2003). Phytoremediation plants for phytoremediation of toxic metals biostimulation trial in semi field conditions. Sci- F of heavy metal-contaminated land by trees - a and metalloids. In: “Transgenic Plant Technol- ence of the Total Environment 686: 484-496. - d

n review. Environment International 29: 529-540. ogy for Remediation of Toxic Metals and Metal- doi: 10.1016/j.scitotenv.2019.05.458 a - doi: 10.1016/S0160-4120(02)00152-6 loids” (Narasimha M, Prasad V eds). Academic Tiller KG (1992). Urban soil contamination in Aus- s e Ramana S, Biswas AK, Singh AB, Ajay Naveen Ku- Press, CA, USA, pp. 319-340. - doi: 10.1016/B978- tralia. Australian Journal of Soil Research 30: c

n mar P, Ahirwar NK, Behera S, Subba Rao A 0-12-814389-6.00015-8 937-957. - doi: 10.1071/SR9920937 e i (2012). Phytoremediation of cadmium contami- Shimp JF, Tracy JC, Davis LC, Lee E, Huang W, Er- Turgut C, Pepe MK, Cutright TJ (2004). The ef- c

s nated soils by tuberose. Indian Journal of Plant ickson LE, Schnoor JL (1993). Beneficial effects fect of EDTA and citric acid on phytoremedia- o Physiology 17 (1): 61-64. [online] URL: http:// of plants in the remediation of soil and ground- tion of Cd, Cr, and Ni from soil using Helianthus e

g www.researchgate.net/publication/236258876 water contaminated with organic materials. annuus. Environmental Pollution 131 (1): 147-154. o i Ramana S, Biswas AK, Singh AB, Ahirwar NK Critical Reviews in Environmental Science and - doi: 10.1016/j.envpol.2004.01.017 B

(2013). Evaluation of phytoremediation ability Technology 23: 41-77. - doi: 10.1080/1064338930 Turner AP, Dickinson NM, Lepp NW (1991). In- – of some floricultural plant species. Plant Physi- 9388441 dices of metal tolerance in trees. Water, Air, t s ology Reports 18 (2): 187-190. - doi: 10.1007/s40 Signes-Pastor AJ, Munera-Picazo S, Burlo F, and Soil Pollution 57-58 (1): 617-625. - doi: e r 502-013-0029-8 Cano-Lamadrid M, Carbonell-Barrachina AA 10.1007/BF00282925 o

F Ramana S, Biswas AK, Singh AB, Ahirwar NK, (2015). Phytoremediation assessment of Gom- Vassilev A, Schwitzguebel J-P, Thewys T, Lelie D, i Rao AS (2015). Tolerance of ornamental succu- phrena globosa and Zinnia elegans grown in ar- Vangronsveld J (2004). The use of plants for re- lent plant crown of thorns (Euphorbia milli) to senic-contaminated hydroponic conditions as a mediation of metal-contaminated soils. The Sci- chromium and its remediation. International safe and feasible alternative to be applied in ar- entific World Journal 4: 9-34. - doi: 10.1100/tsw. Journal of Phytoremediation 17 (4): 363-368. - senic-contaminated soils of the Bengal Delta. 2004.2 doi: 10.1080/15226514.2013.862203 Environmental and Monitoring Assessment Vyslouzilová M, Tlustoš P, Száková J (2003). Cad- Reed ST, Ayala-Silva T, Dunn CB, Gordon GG, 187: 387. - doi: 10.1007/s10661-015-4618-z mium and zinc phytoextraction potential of Meerow A (2013). Screening ornamentals for Sleegers F (2010). Phytoremediation as green in- seven clones of Salix spp. planted on heavy their potential as accumulator plants. Journal frastructure and a landscape of experiences In: metal contaminated soils. Plant Soil and Envi- of Agricultural Science 5 (10): 20-27. - doi: Proceedings of the “Annual International Con- ronment 49 (12): 542-547. - doi: 10.17221/4191- 10.5539/jas.v5n10p20 ference on Soils, Sediments, Water and En- PSE Ribeiro De Souza S, López De Andrade A, Anjos ergy”, vol. 15, Article 13. [online] URL: http:// Waranusantigul P, Kruatrachue M, Pokethitiyook De Souza L, Schiavinato MA (2012). Lead toler- scholarworks.umass.edu/soilsproceedings/vol1 P, Auesukaree C (2008). Evaluation of Pb phy- ance and phytoremediation potential of Brazil- 5/iss1/13 toremediation potential in Buddleja asiatica and ian leguminous tree species at the seedling Solanki P, Narayan M, Rabha AK, Srivastava RK B. paniculata. Water Air and Soil Pollution 193: stage. Journal of Environmental Management (2018). Assessment of cadmium scavenging po- 79-90. - doi: 10.1007/s11270-008-9669-0 110: 299-307. - doi: 10.1016/j.jenvman.2012.06. tential of Canna indica L. Bulletin of Environ- Watharkar AD, Jadhav JP (2014). Detoxification 015 mental Contamination and Toxicology 101 (4): and decolorization of a simulated textile dye Roloff A, Korn S, Gillner S (2009). The climate- 446-450. - doi: 10.1007/s00128-018-2416-3 mixture by phytoremediation using Petunia species matrix to select tree species for urban Stevović S, Mikovilović VS, Calić-Dragosavac D grandiflora and Gailardia grandiflora: a plant- habitats considering climate change. Urban (2010). Environmental study of heavy metals in- plant consortial strategy. Ecotoxicology and Forest and Urban Greening 8 (4): 295-308. - doi: fluence on soil and Tansy (Tanacetum vulgare Environmental Safety 103: 1-8. - doi: 10.1016/j. 10.1016/j.ufug.2009.08.002 L.). African Journal of Biotechnology 9: 2392- ecoenv.2014.01.033 Rosselli W, Keller C, Boschi K (2003). Phytoex- 2400. [online] URL: http://www.ajol.info/index. Wan X, Lei M, Chen T (2016). Cost-benefit calcu- traction capacity of trees growing on metal php/ajb/article/view/78473 lation of phytoremediation technology for contaminated soil. Plant Soil 256 (2): 265-272. - Subhashini V, Swamy AVVS (2013). Phytoremedi- heavy-metal contaminated soil. Science of the doi: 10.1023/A:1026100707797 ation of Pb and Ni contaminated soils using Total Environment 563- 564: 796-802. - doi: Salt DE, Blaylock M, Nanda Kumar PBA, Du- Catharanthus roseus (L.). Universal Journal of 10.1016/j.scitotenv.2015.12.080 shenkov V, Ensley BD, Chet I, Raskin I (1995). Environmental Research and Technology 3 (4): Wang XF, Zhou QX (2005). Ecotoxicological ef- Phytoremediation: a novel strategy for the re- 465-472. [online] URL: http://www.environ fects of cadmium on three ornamental plants. moval of toxic metals from the environment mentaljournal.org/3-4/ujert-3-4-7.pdf Chemosphere 60 (1): 16-21. - doi: 10.1016/j.chem using plants. Nature Biotechnology 13: 468-474. Subhashini V, Swamy AVVS (2014). Phytoremedi- osphere.2004.12.031 - doi: 10.1038/nbt0595-468 ation of metal (Pb, Ni, Zn, Cd and Cr) contami- Wang Y, Yan A, Dai J, Wang NN, Wu D (2012). Ac- Saxena G, Purchase D, Mulla SI, Saratale GD, Sax- nated soils using Canna indica. Current World cumulation and tolerance characteristics of ena G (2019). Phytoremediation of heavy metal- Environment 9 (3): 780-784. - doi: 10.12944/ cadmium in Chlorophytum comosum: a popular contaminated sites: eco-environmental con- CWE.9.3.26 ornamental plant and potential Cd hyperaccu- cerns, field studies, sustainability issues, and fu- Sun Y, Zhou Q (2016). Uptake and translocation mulator. Environmental Monitoring and Assess- ture prospects. Reviews of Environmental Con- of benzo[a]pyrene (B[a]P) in two ornamental ment 184: 929-937. - doi: 10.1007/s10661-011- tamination and Toxicology 249: 71-131. - doi: plants and dissipation in soil. Ecotoxicology and 2010-1 10.1007/398_2019_24 Environment Safety 124: 74-81. - doi: 10.1016/j. Wei SQ, Pan SW (2010). Phytoremediation for Scheyer JM (2000). Estimating dietary risk from ecoenv.2015.09.037 soils contaminated by phenanthrene and soils in urban gardens. In: “Proceedings of the Tao JM, Wang YB, Dai J (2011). Accumulation and pyrene with multiple plant species. Journal of First International Conference on Soils of Ur- tolerance of zinc in ornamental plant Chloro- Soils and Sediments 10 (5): 886-894. - doi: ban, Industrial, Traffic and Mining Areas” phytum comosum. Applied Mechanics and Ma- 10.1007/s11368-010-0216-4 (Burghardt W, Dornauf C eds). Essen (Ger- terials 66- 68: 524-27. - doi: 10.4028/www.scien Wu FZ, Yang WQ, Zhang J, Zhou LQ (2011). many) 12-18 July 2000, vol. 2, pp. 479-484. tific.net/AMM.66-68.524 Growth responses and metal accumulation in Schleu U, Wu Q, Blume H-P (1998). Variability of Tauqeer HM, Ali S, Rizwan M, Ali Q, Saeed R, an ornamental plant (Osmanthus fragrans var. soils in urban and periurban areas in Northern Iftikhar U, Ahmad R, Farid M, Abbasi GH (2016). thunbergii) submitted to different Cd levels. In- Germany. Catena 33 (3-4): 255-270. - doi: 10.1016 Phytoremediation of heavy metals by Alternan- ternational Scholarly Research Network, vol. /S0341-8162(98)00070-8 thera bettzickiana: growth and physiological re- 2011, Art. ID 738138. - doi: 10.5402/2011/738138 Scholz T, Hof A, Schmitt T (2018). Cooling effects sponse. Ecotoxicology and Environmental Saf- Yongpisanphop J, Babel S, Kruatrachue M, and regulating ecosystem services provided by ety 126: 138-146. - doi: 10.1016/j.ecoenv.2015.12. Pokethitiyook P (2017). Hydroponic screening urban trees novel analysis approaches using ur- 031 of fast-growing tree species for lead phytore-

150 iForest 13: 139-151 Phytoremediation in urban areas y

mediation potential. Bulletin of Environment tion. Plant and Soil 249 (1): 139. - doi: 10.1023/A: Zn in contaminated soil. Science of the Total r t

Contamination and Toxicology 99 (4): 518-523. - 1022504826342 Environment 650 (1): 594-603. - doi: 10.1016/j.sci s

doi: 10.1007/s00128-017-2157-8 Zeng P, Guo Z, Cao X, Xiao X, Liu Y, Shi L (2018). totenv.2018.09.055 e r

Zacchini M, Pietrini F, Scarascia Mugnozza G, Iori Phytostabilization potential of ornamental Zhang CP, Qui S, Zhao J, Li XJ, Quan YB (2010). o F V, Pietrosanti L, Massacci A (2009). Metal toler- plants grown in soil contaminated with cad- Phytoremediation properties of three orna- d

ance, accumulation and translocation in poplar mium. International Journal of Phytoremedia- mental plants for cadmium absorption in soils. n a and willow clones treated with cadmium in hy- tion 20 (4): 311-320. - doi: 10.1080/15226514.20 Journal of Guangxi Agricultural Science 41 (10): s

droponics. Water Air and Soil Pollution: 23-34. - 17.1381939 1101-1103. [online] URL: http://www.cabdirect. e c

doi: 10.1007/s11270-008-9788-7 Zeng P, Guo G, Xiao X, Peng C, Feng W (2019). org/cabdirect/abstract/20113030693 n e

Zayad AM, Terry N (2003). Chromium in the envi- Phytoextraction potential of Pteris vittata L. co- i c

ronment: factors affecting biological remedia- planted with woody species for As, Cd, Pb and s o e g o i B

–

t s e r o F i

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