BiomassandBioenergy83(2015)328e339 ContentslistsavailableatScienceDirect Biomass and Bioenergy journal homepage: http://www.elsevier.com/locate/biombioe Review Integrating phytoremediation with biomass valorisation and critical element recovery: A UK contaminated land perspective Ying Jiang a, Mei Lei b, Lunbo Duan c, Philip Longhurst a,* aCentreforBioenergy&ResourceManagement,SchoolofEnergy,Environment&Agrifood,CranfieldUniversity,Cranfield,MK430AL,UK bCentreforEnvironmentalRemediation,InstituteofGeographicSciencesandNaturalResourcesResearch,ChineseAcademyofSciences,Beijing,100101, China cKeyLaboratoryofEnergyThermalConversionandControl,MinistryofEducation,SchoolofEnergyandEnvironment,SoutheastUniversity,Nanjing, 210096,China a r t i c l e i n f o a b s t r a c t Articlehistory: IntheUK,thewidespreadpresenceofelementalcontaminantssuchasarsenicandnickelincontami- Received27May2015 natedsitesandmorewidelyreleaseofplatinumgroupmetalsintothebiospherearegrowingconcerns. Receivedinrevisedform Phytoremediation has the potential to treat land contaminated with these elements at low cost. An 30September2015 integratedapproachcombininglandremediationwithpost-processbiomasstoenergyconversionand Accepted14October2015 highvalueelementrecoveryisproposedtoenhancethefinancialviabilityofphytoremediation. Availableonline24October2015 Ananalyticalreviewofplantspeciessuitableforthephytoremediationofnickel,Arsenicandplatinum groupmetalsisreported.Additionally,apreliminarymodelisdevelopedtoassesstheviabilityofthe Keywords: proposedapproach.AfeasibilityappraisalusingMonteCarlosimulationtoanalyseprojectrisksuggests Phytoremediation Elementalcontaminant highbiomassyieldplantspeciescansignificantlyincreasetheconfidenceofachievingfinancialreturn Biomasstoenergy fromtheproject.Theorderoffinancialreturnfromrecoveringelementswasfoundtobe:Ni>Pt>As. Montecarlosimulation CrownCopyright©2015PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense Riskanalysis (http://creativecommons.org/licenses/by/4.0/). Contents 1. Introduction................................................................ ...................................................... 328 2. Phytoremediationandplantselection.................................................... ............................................ 329 2.1. Arsenicphytoremediation.....................................................................................................330 2.2. Nickelhyperaccumulators.....................................................................................................331 2.3. PGMphytoremediation .......................................................................................................332 3. Improvementoffinancialfeasibilityofphytoremediationprojectbyplantbiomassutilisationandelementrecovery.............. ............ 333 3.1. Economicmodelofaphytoremediationproject ........................................... ......................................335 3.2. Riskmanagementoftheintegratedphytoremediationproject .................................... ................................337 4. Conclusion ................................................................ ....................................................... 338 Acknowledgement ............................................................ ....................................................338 References.........................................................................................................................338 1. Introduction identifiedelementalcontaminants,Arsenic(As)andnickel(Ni)are twoofthemostcommonones.Duetotheirubiquitousoccurrence Soilscontaminated with metaland metalloidelements pose a on contaminated sites, concentration levels and high risk factors, major environmental and human health risk. Amongst the bothelementsarelistedaspriorityinorganiccontaminantsunder theUKPart2Aregime[1].Platinumgroupmetals(PGMs)onthe otherhand,haveonlylimiteddistributionintheenvironmentand * Correspondingauthor. inertchemicalandbiochemicalproperties;thereforehavenotbeen E-mailaddress:P.J.Longhurst@cranfield.ac.uk(P.Longhurst). http://dx.doi.org/10.1016/j.biombioe.2015.10.013 0961-9534/CrownCopyright©2015PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/). Y.Jiangetal./BiomassandBioenergy83(2015)328e339 329 recognisedasprioritysoilcontaminants.However,theincreasing translocatecontaminantstoabove-groundtissuesforlaterharvest, useofPGMsinthepastfewdecadesinvehicleexhaustcatalysts,as i.e.phytoextraction;convertingtheelementtoalesstoxicchemical wellasinseveralotherindustrialandmedicalapplicationshasled species, i.e. transformation; or at the very least sequestering the to a heightened soil concentration of PGMs, especially in urban elementinrootstopreventleachingfromthesitei.e.phytostabi- high-trafficareas[2]aswellashighvaluelossesinminingareas. lisation.Asacompetingtechnology,phytoremediationoffersalow Consequently, these increases have given rise to public health cost,albeitsloweralternativetophysicalandchemicaltreatment concerns[2]. methods[9]andisviableinmitigatingcontaminationlevelsfora IntheUK,metalsandmetalloidsarethemostwidespreadsoil widerangeoforganicandinorganiccontaminants.However,asa contaminantspresentinover80%ofallidentifiedsitesinEngland biological method, phytoremediation is limited by a number of and Wales [3]. Management and remediation of these sites is factors such as the long treatment time and site/contaminant clearlyofpublicinterest.Fromanenvironmentalperspectiveitis specificityetc. In addition, a key inhibiting factor for commercial desirabletorehabilitatecontaminatedsitestothehighestpossible implementation of phytoremediation is the disposal of large standard, regardless of the potential costs. In practice, such ap- quantitiesofcontaminatedplantbiomassmaterialthataccumulate proachesimposeaheavyfinancialburdenongovernmentexpen- throughouttheprocess[10,11].Whencontaminantconcentrations diture, as demonstrated by the Dutch government since their in the biomass exceed specific levels, the biomass material is adoptionofthisapproachintheearly1980s.AccordingtoHonders regarded as potentially hazardous, therefore must be stored or etal.[4],itwasestimatedthatifalltheidentifiedsitesinHolland disposedofappropriately[12].Here,aradicalapproachtoaddress were treated to the standard required by legislation, the total thisdisposalproblembyincorporatingathermochemicalconver- remediationcostswouldbeintheorderof50billioneuros.By1997, sionofbiomasstorenewableenergyfollowedbyametal(loid)re- itwasevidentthatthe‘Dutchsystem’wasnotfinanciallysustain- covery stage to the process is proposed. The feasibility of using able and the government changed their system to a more cost- phytoremediationtechnologytoremediateselectedelementsfrom effective ‘function-orientated’ approach adopting a risk-based contaminatedsiteswhicharenotonthelocalauthorities'priority managementsystem,similartotheUK[5]. listisreviewed,thenfollowsdiscussionofthefeasibilityofsuchan UKcontaminatedlandisregulatedbyaframeworkoflegislation integrated approach to maximise economic benefit from phytor- and policies underpinned by the contaminated land regime (as emediation alongside biomass energy production and high value stipulatedinPart2AoftheEnvironmentalProtectionAct1990,or metalrecovery. simplyPart2A)andland-useplanningregimeWithinthisregime theTownandCountryplanningAct1990isthemostimportant). 2. Phytoremediationandplantselection The underlying concept of the UK system emphasises on a risk- basedapproach[6]andrelianceontheland-useplanningsystem Phytoremediation asadisciplinein environment scienceswas (87%inEnglandand79%inWales)tofundremediationworkwhen established in late 1970s following the discovery of a series of the site is developed and redeveloped [3]. This approach, in hyperaccumulators [13]. Since then the field has developed contrasttothe‘Dutchsystem’hasprovedtobemorecost-effective attractingnotonlyscientificinterestbutattentionfromprivateand forgovernmentintervention.Howeverthisapproachislimitedto industrial site owners, regulators and the environmental engi- urbanareaswherethereisarapidlyexpandinglandrequirement neeringcommunity[9].Todate,intensiveresearchinthisareahas for residential and commercial development, and no lack of resulted in a significant improvement in knowledge of hyper- financial drive for developers to undertake remediation work. In accumulators and their elements of affinity. It is now generally ruralandlowervalueareaswherecommerciallanddevelopmentis agreedthatinordertodistinguish‘hyperaccumulator’fromnormal less competitive, there remain a large number of contaminated oraccumulator,asetof thresholdvaluesofelementalconcentra- siteswithremediationworkpendingduetofinancialbarriers.Ac- tions in plant biomass (dry weight) are used to define hyper- cording to the latest survey carried out by UK Environmental accumulation:MnandZnhyperaccumulatorscontain>10,000mg/g Agency,bytheend of2007,of the746contaminatedsiteswhich [14],hyperaccumulatorsofAs,Co,Cu,Ni,Se,andPbhave>1000mg/ had been identified under Part 2A, only 144 were reported as g[14,15],andhyperaccumulatorsofCdhave>100mg/g[14]. completelyremediated[3]. The mechanism and rationale of phytoremediation has been Remediation of elemental soil pollutants presents distinct sci- discussed in a number of reviews [16e20]. Depending on con- entificandtechnicalchallenges,asunlikeorganicpollutantsthese taminants, the siteconditions, level of clean-up requiredand the cannotbedegradedfurtherintonon-harmfulproducts.Therefore plantspecies,itinvolvestheuseofplantstoextract,sequester,and/ theonlywaytoremediatetoxicelementalpollutantsistoremove ordetoxifypollutants[21].Theconceptofusingplantstouptake orsequesterthemfromthesoil.Currenttechnologiesavailablefor environmental contaminants from soil is not new, however it is remediation of elemental pollutant including in-situ or ex-situ onlyinthetwentiethcentury,afteraseriesofdiscoveryofhyper- chemicaltreatment,biologicaltreatment,soilwashing,soilflush- accumulator and vast advance of analytical techniques, has the ing,vitrification,incinerationandlandfilling[7]. conceptofphytoremediationbeenrapidlydeveloped[14]. Remedial treatments for contaminated sites in the UK are In recent years, research on phytoremediation has shown the currentlydominatedbyexcavationandoff-sitedisposalofmaterial. overallenvironmentalandeconomicbenefitsfromlandremedia- Thispractice isusedalmostexclusivelyforremedialwork of this tion.Currentresearchtrendsarefocusingonmaximisingtheuseof typeandregardedasthelikelysolutionforallfutureworkinthe by-products fromphytoremediationprocess.Researchersarealso view of Environmental Agency [3]. Preference for this ‘dig and exploringtheusephytoremediationbiomassasarenewableenergy dump’approachisduetoitsstraightforwardoperationandshort source [22,23]. In addition, the concept of moving from ‘phytor- project time frame. However, volatile emissions, odour nuisance emediation’ to ‘phytomining’ to reclaim potentially valuable ele- andnoiseduringtheexcavationstageaswellaspossiblesecondary mentsforfurthereconomicbenefitsisunderway. contamination during transport and landfill are evident risks. In The greatest advantage of phytoremediation is low cost. Ac- additiontotheenvironmentalconcern,increasinglandfilltaxation cordingtoaEuropeanscalestudy[7],theaveragecostforon-site resultinthismethodnotbeingvariable/feasibleinthelongterm phytoremediation and off-site landfilling are 122 and 231 Euro [8]. perm3,respectively.IntheAmericanmarket,similarcostadvan- Phytoremediation technology uses plants to extract and tagesfromphytoremediationexist.Itisgenerallyagreedthatthe 330 Y.Jiangetal./BiomassandBioenergy83(2015)328e339 estimated cost for phytoremediation of soil is in the range of largelyattributedtotheproductionofintracellular thiolssuchas 25e100 US dollars per ton [9], in contrast to approximately glutathione (GSH) and phytochelatins (PCs) which are chelators 150e350 US dollars per ton for conventional excavation-landfill withastrongaffinitytoarsenic[29e31]. approaches [24]. In addition to the cost, phytoremediation offers Among the numerous arsenic hyperaccumulating plants re- better performance compared to the conventional approach, e.g. ported to date, the majority belong to the fern Pteris family permanentlyremovalofthecontaminants,lessdisturbancetothe (Table1).ThefirstarsenichyperaccumulatorPterisvittatawasre- site. It has to be noted that phytoremediation will more readily portedin2001byMaetal.[15].Theplantisamesophyticfernthat remove the bioavailable fraction of the contamination, and is capableofaccumulatingarsenicintheabovegroundfrondwithin therefore more compatible with risk-based contaminated land the range of 2500e22,630 mg kg(cid:1)1 on a dry weight (DW) basis, management systems [9]. The common perception towards dis- ~100-fold higher than soil concentrations [15,28]. This discovery advantages of phytoremediation is the substantially longer time has led to intensive screening of the fern Pteris family for other scalesrequiredforremediationtobecompleted.Thisdisadvantage potential arsenic hyperaccumulators [28,32]and as a result, a hasexcludedphytoremediationasamainstreamtechnologysolu- number of species in the family such as Pteris cretica and Pteris tionforurbancontaminatedsites.Itshouldalsobenotedthatthe umbrosa,havebeenrecognisedasarsenichyperaccumulators. specificity of hyperaccumulators result in selective remediation The high BF, TFand reasonable biomass yield of P. vittata has whichislesseffectiveforsiteswithmultiplecontaminants[25]. prompted notable attention from commercial phytoremediation Selectingtherightplantsforphytoremediationfromthewide projects.Fieldstudieshavebeenconductedonanumberofocca- rangeofcandidatesisthemostimportantstageofsuchproject.In sions.Grayetal.[26]demonstratedinfieldstudiescarriedoutin generalruleachievingahighbioaccumulationfactor(BF,definedas southwestEnglandthatP.vittataandP.creticaarebothsuitablefor theratioofelementconcentrationinplantbiomasstothatinsoil) climateconditionsinthatregion.Afterexposureofsoiltotalarsenic andhightranslocationfactor(TF:definedastheratio ofelement concentrationsof471mgkg(cid:1)1,bothspeciesexhibitedahigheffi- concentration in above ground shoots to that in roots) is key. ciency of bioaccumulation and root to shoot translocation, with However,whenlandremediationisnotthesolegoaloftheproject most of the arsenic accumulated in the frond (4371 and and downstream processes for element and energy recovery are 2344mgkg(cid:1)1forP.vittataandP.cretica,respectively.)Howeverthe desired,otherfactorssuchashighbiomassyieldandtoleranceto relatively low above ground biomass yield from P. vittata which the contaminants also become relevant. The rationale to support averagedat0.76tha(cid:1)1of(ondryweighbasis)hasbeenconcluded thisdecisionmakingisdiscussedinthefollowingsection. tobe the maindrawbackforachieving higharsenicextraction in thefieldstudy. 2.1. Arsenicphytoremediation Kertulis-Tartaretal.[33]carriedouta2-yearfieldstudyusing P. vittata for phytoremediation of the soil contaminated with Arsenic is a metalloid which is considered non-essential and chromated copper arsenate on a 30.3 m2 plot. Soil arsenic con- toxic at high concentration to plants and animals. In the UK, centrationsatthebeginningofthestudyweremeasuredbetween particularly in the Southwest, large areas of soil are considered 190 and 278 mg kg(cid:1)1 from samples taken at depths within the contaminatedwithAs,eithergeogenicallyorfromanthropogenic rangeof1e60cm.Duringthe2-yrperiod,atotalof26.3gofarsenic activities such as mining and smelting [26]. In other part of the wasremovedfromtheplot.Reportedbiomassyieldwasapproxi- world, Arsenic-contaminated soil is one of the major sources of mately 1.3 t ha(cid:1)1. This improved yield was possibly due to the arsenicindrinkingwater[27],andalsoresultsinhigharseniclevel subtropical climate in Florida where the test was carried out. incereals,vegetablesandfruitsgrownonthecontaminatedsoil.All Similarly,elevatedbiomassyieldhavealsobeenreportedbyChen chemicalspeciesofarsenicarebioactive[28]andthereforecanbe etal.[34]inafieldstudycarriedoutinasubtropicalclimateregion, readilyabsorbedbyanimalsandplants.Thisbiochemicalproperty in which an average above ground biomass yield of just below ofarsenicgivesrisetointensiveresearchintohyperaccumulators 2tha(cid:1)1wasachieved. which can be applied for the phytoremediation of arsenic. A Biomassyieldofthepollutantaccumulatorsisthedetermining numberofstudiesreportthattheabilitytotolerantandaccumulate factorforthesuccessanddurationofthephytoremediationprocess arsenic in many plant and phytoplankton species. This can be [35]. For P. vittata, although it has a significantly higher biomass Table1 Plantspecieswithpotentialforarsenicphytoremediation. Species Planttype Reportedaccumulationrates(mgkg(cid:1)1DWa) Reference AgrostiscaninaL. Perennialherbb 460 [40] AgrostisstoloniferaL. Perennialherb 1350 [40] AgrostistenuisSibth. Perennialherb 3470 [40] Callunavulgaris Perennialshrub 4131 [40] Helianthusannuus Annualherb 1550 [39] Holcuslanatus Perennialherb 560 [32,40] JasionemontanaL. Annual/biennialherb 6640 [40] Pityrogrammacalomelanos Fern 5000e8350 [67] PterisbiauritaL. Fern 2000 [68] Pteriscretica Fern 3500e4000infrond;2200e2600inroot [28,32] Pterislongifolia Fern 4308 [28,32] Pterisquadriaurita Fern 2900 [68] Pterisryukyuensis Fern 3700 [68] Pterisumbrosa Fern 3735e5000 [28,32] Pterisvittata Fern 2500e22,630 [15,28] Reynoutriasachalinensis Perennialshrub 1900 [69] Note. a DW¼DryWeight. b Herb¼Herbaceousplant. Y.Jiangetal./BiomassandBioenergy83(2015)328e339 331 yieldcomparedtomostofthehyperaccumulators,itisstillfarless than those of high yield economic crops such as sunflower and cultivarsinthewillowfamily. Shelmerdineetal.[36]examinedthesuitabilityofP.vittatafor phytoremediationof21siteshistoricallycontaminatedwitharsenic atvariouslevelsaroundEngland.Thestudyfoundthatthefraction ofAsremovedgenerallydeclinedassoilAsconcentrationincreased. Anuptakemodelwasdevelopedusingexperimentaldatatopredict the time frame required for site cleanup to the target level. It is concludedbytheauthorsthatP.vittataisonlysuitableforsoilswith minorlevelsofarseniccontaminationandthatmajorlimitationto successfulphytoremediationislowbiomassyieldofP.vittata. Increasingly, research evidence suggests that although species in the Pteris familyexhibit a high capacity of bioaccumulation of arsenic,thelowbiomassP.vittataproductionhindersitsapplica- tion on heavily contaminated sites [37,38]. High yield common plantsandeconomiccrops,ontheotherhand,havebeendemon- strated in a number of studies to have more promising field application[38e40]. Amongtheplantspeciesproposedinthesestudies,shrubwil- low (Salix spp.) and sunflower (Helianthus annuus) are the most promising for phytoremediation field applications due to their relativelyhighaccumulationabilityandsubstantialbiomassyield. According toJanuaryetal. [39] H.annuus is capableof uptake of arsenic upto1550 mg kg(cid:1)1 in the plant shootunderhydroponic conditions.ThestudyalsosuggestsH.annuusiscapableofhyper- accumulatingsimultaneouslyarangeofothermetalcontaminants suchasnickel,cadmiumandchromium.Anumberofrecentstudies have addressed the potential of Salix spp. for a range of phytor- emediation applications [38,41]. Purdy and Smart [38] examined Fig.1. NiconcentrationintopsoilinEnglandasapercentileclassifiedinterpolated arsenicaccumulationaffinityinfourwillowclonesgrownhydro- image. ponically.Inthehighestaccumulatingclone,arsenicwasaccumu- Source:DefraTechnicalGuidanceSheetNo.TGS05[45]. lated at 329, 201 and 5800 mg kg(cid:1)1 in the leaf, stem and root, respectively.Inasimilarhydroponicstudy,Puckettetal.[41]found other hyperaccumulators [14]. The plant family most strongly accumulation of an As-tolerant willow (Salix viminalis (cid:3) Salix represented are Euphorbiaceae, Brassicacceae, Asteraceae, Fla- miyabeana) reached 66.8, 34.2, and 3170 mg kg(cid:1)1 and an As- courtiaceae,BuxaceaeandRubiaceae[14].Table2selectivelylistsa sensitive willow (Salix eriocephala) reached 20.3, 16.8, and number of plant species with potential for application inphytor- 2380mgkg(cid:1)1(DW)forleaf,stem,androot,respectively. emediationprojects.Detailedsummariesofspeciescanbefoundin Although it seems the arsenic accumulation abilities of these earlier works by Baker and Brooks [46], Reeves et al. [47,48] and plantsare2e3timeslessthaninP.vittata,thesignificantlyhigher ReevesandBaker[14].Thereasonforthelargenumberofnickel biomass yield (at least 10e20 fold) drastically reduces the reme- hyperaccumulatorsispartiallyduetotheextensiveanalyticalwork diationtime.Itisalsorecognisedthatbiomassproducedduringthe carriedoutonultramaficfloras,butmorefundamentalexplanation phytoremediation process can be reconsidered as a locally pro- canbeattributedtomillionyearsofevolutionofplantscolonisedin duced,renewablefeedstockforbioenergyandbioproducts[42]. theNi-enrichedultramafic,whichisbyfarthemostwidespreadon aglobalscale[14]. 2.2. Nickelhyperaccumulators Theextensivedistributionofnickelinsoilandthelargeselec- tion of nickel hyperaccumulators has encouraged intensive IntheUK,nickelwaschosenasoneoftheeightcontaminants research for phytoremediation of land contaminated by nickel. examined by a study conducted by the British Geological Survey Additionally, the high biomass yield and high bioaccumulation (BGS)inordertogivefurtherguidanceontherecentlypublished factorsexhibitedinsomeofthenickelhyperaccumulatorsmakesit revised Part 2AContaminated Land Statutory Guidance [43]. It is possibletousetheseplantstoextractnickelfromlowgradenickel alsorecognisedbytheEnvironmentalAgencyasoneofthefiftysix oreswhichcoverlargeareasoftheEarthcrust[49]. prioritycontaminantsintheUK[44]. Amongst hundreds of nickel hyperaccumulators, there are a DistributionandconcentrationofnickelintheUKsoilisinflu- numberofspeciesthathavesofarbeenappliedinfieldstudiesand encedmostlybytheunderlyinggeology,i.e.parentmaterialofsoil; have demonstrated their potential for commercial phytor- whereasnickelpollutioninsoilcausedbyhumanactivityisnotas emediation and phytomining. Alyssum bertolonii was reported by significantasseenwithsomeothercontaminants[45].Inarecent Robinsonetal.[50]inafieldtrialascapableofaccumulatingNiat studyconductedbyBGS[43,45],significantlyhighconcentrations 0.8%(8gkg(cid:1)1)drymatterofitsbiomass.Reasonablygoodbiomass of nickel wereidentified in areas at the southern tip of Cornwall yield was achieved with moderate fertilization (N, P and K) at (Lizardserpentinites),ironstonerockrichareasinOxfordshireand 9.0 t ha(cid:1)1, which gave a metal yield of 72 kg ha(cid:1)1 assuming all areasinthePeakDistrictwheremineralisationandNi-richparent nickelinthebiomassisrecovered.Theauthorsconcludedthatthe materialareresponsibleforhighNiconcentrationinsoil(Fig.1). net return from this Ni hyperaccumulator per hectare could be Sincethediscoveryoftheworld'sfirst‘nickelaccumulator,sofar comparable tothatof wheat based ona conservative calculation. no less than 320 plant species have been reported, which makes However if energy yield from biomass via thermochemical con- nickel hyperaccumulators possibly the largest family amongst version,e.g.gasificationisconsidered,evenhigherreturnscanbe 332 Y.Jiangetal./BiomassandBioenergy83(2015)328e339 Table2 Plantspecieswithpotentialfornickelphytoremediation. Family Species Planttype Reportedaccumulationrates(mgkg(cid:1)1 Reference DW) Asteraceae Berkheyacoddii Perennialherb 11,600 [51] Berkheyazeyheri Perennialherb 17,000 [47,48] Pentacalia(10species) Herb 16,600 [47,48] Helianthusannuus Annualherb 510e1070 [39,70] Seneciocoronatus Herb 24,000 [71] Brassicaceae Alyssum(48taxa,allinsectionOdontarrhena) Annualorperennialherbs 1280e29,400 [46,72,73] Bornmuellera(6taxa) 11,400e31,200 [48,74,75] Thlaspi(23taxa) Annualorperennialherbs 2000e31,000 [48] Buxaceae Buxus(17taxa) Shrub 1320e25,420 [47] EuphorbiaceaeLeucocroton(27species) Herbs 2260e24,600 [76] Phyllanthus(16taxa) Herbs 1090e38,100 [77] Phyllanthuschamaecristoides(2subsp:chamaecristoidesand Herbs 3400e31,740 [47] baracoensis) Cleidionviellardii Herbs 9900 [48] Baloghiasp. Herbs 5380 [48] Flacourtiaceae Homalium(7species) Shrub(withinwillow 1160e14,500 [78] family) Xylosma(11species) Shrub(withinwillow 1000e3750 [78] family) Rubiaceae Psychotriadouarrei Shrub 14,900e27,700 [79] achieved.Inalaterstudycarriedoutbythesameresearchgroup exposedto5.7mgl(cid:1)1Pt.Duringasix-weekexposuretothePt,an [51],ahighbiomassyieldNihyperaccumulatorBerkheyacoddiiwas accumulationfactorof6952intherootswasachieved. reported. In the field test, the plant was capable of accumulating Ballach and Wittig [57] carried out a hydroponic experiment 1.8e7.8 g kg(cid:1)1 Ni in the above ground biomass (on dry weight usingpoplar(Populusmaximowiczii)toexaminetheaccumulation basis)whilstachieving22tha(cid:1)1ofdrybiomass.Additionally,the ofPtanditstoxiceffectonbiomassgrowth.Thegrowthnutrient ease of propagation and culture, as well as its tolerance to cool solutionwasspikedwith34.8mgl(cid:1)1PtCl4.Thestudyagreedwith climaticconditionrenderthisspeciesasuitableagentforphytor- previousliteraturethatthePtwaspredominatelyaccumulatedin emediationparticularlyintheUK.Theeconomicaspectsofusing therootandthetranslocationfactortootherpartsofthetissuewas B.coddiiarediscussedbytheauthorsinthisstudy.Itisconcluded verylimited.Howevertheauthorsnotedthattheaccumulationof thatatthehighestNiconcentrationinthebiomassarchivedinthis Ptsimultaneouslycausedagradualdepletionoftheplants’water study(7.8gkg(cid:1)1),1haofB.coddiicropcanremove168kgofNi supply. assuming the biomass yield of 22 t ha(cid:1)1. When combined with DuetothestablechemicalandbiochemicalpropertiesofPGMs, energy from biomass combustion, assuming at 25% of the total bioaccumulation of these elements from soil by plants is heavily biomasscalorificvalue,anestimatedreturnofUS$1548perhais dependent on their chemical forms. Despite this, hydroponic ex- predictedbytheauthorsatthetimethestudy. periments where plants were exposed to high concentrations of dissolved Pt-salts can provide insight of metal distribution after 2.3. PGMphytoremediation uptake.Inordertoassessthefeasibilityofphytoremediation/phy- tomining of PGMs as a commercially viable option, experimental In the UK, PGMs such as Pt and Pd are not listed as soil con- datacollectedfromrealisticfieldconditionsisofhighimportance. taminantsinthePart2Aregime.Howeverduetothewideusageof Todate,onlyalimitednumberofstudieshavebeenconductedto catalyticconvertor,highlevelofthesemetalsinroadsidesoiland sufficientlysimulate naturalconditions.HelmersandMergel[58] roaddusthavebecomeagrowingconcern.Studieshaveidentified analysed PGM concentration in grass samples collected within in soils,dusts andplantsexposedtohigh-trafficdensity,concen- close radius of highways and monitored the concentration trend trationsofPGMsfarexceedingnaturalbackgroundlevels[52].Long overa3-yearperiod.ItwasfoundthataverageconcentrationsofPt termmonitoringoftheseenvironmentalsamplesshowsanupward increasedfrom3.6to10.6mgkg(cid:1)1andRhfrom0.65to1.54mgkg(cid:1)1. trend of PGM concentration and a strong correlation with traffic The study also reported one particular sample which exposed to conditions[53]. streetdustforamuchlongerperiod,thatcontained96mgkg(cid:1)1(Pt) AutomobilederivedPGMsreleasesaremainlyintheoxidation and15mgkg(cid:1)1(Rh)nearly10timeshigherthanaverageconcen- statusofzeroorasoxide[54];thereforearecommonlyassumedto trationlevels. be inert and immobile in the environment. However solubility In a greenhouse experiment, Scha€fer et al. [59] investigated studiesofexhaustfumeandroaddustssuggestPGMsofsuchorigin concentrationsofPt,RhandPdinplantsgrownoncontaminated areatleastpartlysolubleandthereforemobileintheenvironment highways soils. The PGM concentrations analysed in plants (dry [55].Todate,littleisknownaboutthebiologicalmechanismofhow material) reached upto 8.6,1, and 1.9 mg kg(cid:1)1 for Pt, Rh and Pd, thesenoblemetalsinteractwithplants. respectively.Theorderofuptakeratesforthethreeelementsinall A few early works which studied bioaccumulation rates and plantstestwerefoundtobe:Pd>Pt(cid:4)Rh. effects of platinum by plants were carried out under hydroponic MostoftheexistingliteratureconcerningplantuptakeofPGM conditions. discussesthequestiononlyinthecontextofeffectsoftheirrelease Pallas and Jones [56] have exposed 9 horticultural important tothebiosphere.Totheauthors'bestknowledge,onePGMuptake crops to 0.057,0.57and 5.7mg l(cid:1)1 Ptin a Hoaglandnutrient so- study was carried out in context of phytoremediation/phytoex- lution.AllspeciesaccumulatedasignificantlyhighamountofPtin tractionunderfieldconditions.Nemutandanietal.[60]examined their roots. For cauliflower and tomato in particular, the Pt con- the bioaccumulation capability of an indigenous species B. coddii centration exceeds 1000 mg kg(cid:1)1 on dry weight basis when grown on contaminated land where platinum and palladium Y.Jiangetal./BiomassandBioenergy83(2015)328e339 333 concentrationswere0.04±0.03and0.18±0.07mgkg(cid:1)1(ondry 3. Improvementoffinancialfeasibilityofphytoremediation weightbasis),respectively.Platinumwasfoundaccumulatedinthe projectbyplantbiomassutilisationandelementrecovery leavesandrootsat0.22±0.15and0.14±0.04mgkg(cid:1)1dryweight, respectively. The concentrations of palladium in the leaves and CurrentlyintheUK,thehighlandvaluesinurbanareasarethe roots were 0.71 ± 0.52 and 0.18 ± 0.07 mg kg(cid:1)1 dry weight, drivingforcefordeveloperstoremediatecontaminatedsitesunder respectively.DuetothelackofPGMcontaminatedsitesanddiffi- theplanningsystem.Whereasinmanyareasawayfromprofitable cultyofanalysis,phytoremediationofthesevaluableelementsare land development, funding for remediation is limited. Conse- certainlynotintensivelystudiedcomparedtootherelementssuch quently, a large number of contaminated sites are left untreated. asarsenicandnickel.ThestudyusingB.coddiiasaccumulatorfor According to the latest report published by Environment Agency uptake of PGM demonstrats the potential of phytoremediation/ [3], by 2007 only 18.4% of the determined contaminated sites in phytoextractiontechnologyforremediationandmoreimportantly England and Wales have been remediated. Additionally, the ma- recoveryofthesescarcemetals. jority of these contaminated sites were dealt with through the Fig.2. Logicflowchartoftheproposedintegratedphytoremediationproject. 334 Y.Jiangetal./BiomassandBioenergy83(2015)328e339 Fig.3. Determinantsfortheeconomicmodelofintegratedphytoremediation. planning system and it was estimated only 10% was dealt with levels of metal(loid)s in soil within biomass tissues. Additionally, under Part 2A. Following the gradually reduced government largequantitiesofbiomassproducedduringphytoremediationare funding for contaminated land and the announcement of the amixtureofhemicellulose,cellulose,ligninandminoramountsof closingoftheContaminatedLandCapitalProgramme(CLCP)atthe other organics, which contains substantial amount of calorific endof2013,itislikelythesesiteswillberemainuntreatedinthe value.Whentreatedthermochemically,e.g.throughgasificationor futureandcontinuetoposerisktoecosystemandpublic. pyrolysis,rapidvalorisationcanbeachievedtoprovidefuelgasthat Thereis,therefore,anurgentrequirementforfinanciallyviable canbeusedforheatandelectricitygeneration[64].Themetal(loid) technologieswhichofferfinancialincentivetoremediatecontam- contentinprocessashretrievedatthethermochemicalprocessis inatedsitesoflowlandvalue.Asmetal(loid)sarethepredominant furtherconcentratedcomparedtoitsconcentrationintheoriginal soil pollutants, phytoremediation offers an opportunity for site biomass, due to the efficient bulk reduction during the thermo- withsuchpollutantswhichlackfundingtocarryoutremediation chemical process. Therefore recovery of these elements can be work. muchmorecost-effective,whistavoidingthedisposalcostforlarge From a resource security perspective, most of the metal(loid) quantitiesofpotentiallytoxicbiomass. soil contaminants are alsovaluable natureresources, which have Here we propose an integrated phytoremediation concept been dispersed throughout the environment via industrial and coupling remediation with renewable energy production from commercial activities in much lower concentrations than their biomass and subsequent metal(loid)s recovery. Each of the inte- naturaldeposits.Ithasalreadybeenrecognisedthattherecoveryof gratedstagesandtheirinteractionsareillustratedintheflowchart theseelementsiscriticalforthesustainabilityofindustrialdevel- below(Fig.2). opment,asnaturalreservesaredepletinga.Arsenicispredictedto From an environmental perspective, integrated phytor- berunoutbetween5and50yeariftheconsumptioncontinuesat emediation addresses both land contamination and renewable present rates [61]. Nickel and PGMs are also identified as critical energy demand simultaneously. However, as the remediation in- materialstothe UKeconomyatriskofdepletioninthe Resource dustryislargelymarket-driven,itisessentialtoassesswhetherthis SecurityActionPlan(RSAP)[62].However,despiteincreasingde- approach is financially viable. Furthermore, optimisation of the mand,noneofthissupplyissupportedbyrecycling[63];duetothe profitabilityof this approach is key. Following this, a preliminary highcostofrecoveryfromlowconcentrationswhencomparedto model is defined to analyse the profitability of a single biomass conventionalmining.Thus,lowcosttechnologiesthatofferhigher harveston1haofcontaminatedland.Guidancefrompriorresearch economicincentiveraisecommercialinterest. isusedwithinthemodeltoassesstheprofitabilityofanintegrated Phytoremediation technology satisfies both requirements for landremediationprojectforvariousscenarios,i.e.targetelement lowcostlandclean-upandelementrecoverybyconcentratinglow andplanttype.Itshouldbenotedthattheresultsfromthemodel Y.Jiangetal./BiomassandBioenergy83(2015)328e339 335 Table3 financialreturnfromcropproductionfromthelandafterremedi- Deterministicparametersofthemodel. ation has been achieved. The work demonstrated the economic Symbol Parameter Value benefitof thephytoremediationbysubsidisingthecostofselling biomass alongside the potential long-term income from the Vth Heatfeedintariff(£/kWh) 0.01a Ep Costofgrowingplantsperhectare(£/ha) 245b cleaned area. However, this model offers only limited immediate Es Costofmetalsmelting£/kg 0.4b incometothestakeholder,asremediationcantakedecadesforthe Vm MarketvalueofAs(£/kg) 0.88 soiltoreachasuitableconditionforgrowingcommercialcrops. MarketvalueofNi(£/kg) 8.69 Robinson et al. [50] calculated the required biomass for a MarketvalueofPt(£/kg) 27,086.6 hyperaccumulator having a metal content of 1% (on dry weight a Sourceofdata:DepartmentofEnergy&ClimateChange,UK.http://chp.decc. basis)toachieveafinancialreturnof500USdollarssolelyfromthe gov.uk/cms/renewable-heat-incentive/. recoveredmetal.Thestudyconcludedthatundertheassumption b Sourceofdata:Grayetal.[26]. thataverageannualbiomassyieldof30t/ha,onlycobalt,nickel,tin, are not intended to provide an accurate estimation of financial cadmium,manganeseandnoblemetals(Au,AgandPtetc.)would return; rather to provide an insight into how decision on plant befinanciallyviable. selection and the prioritised targetelement can affect the profit- Clearlythereareeconomiclimitsintermsofbiomassproduc- abilityandoverallfinancialriskofsuchaproject. tionandmetalcontentwhenusingphytoremediationformetal(- loid)elementrecovery.Whenonetakesintoconsiderationenergy 3.1. Economicmodelofaphytoremediationproject productionandlandreclamation,theoverallenvironmentalben- efitsincreasethusaffectingtheoverall economicbalanceofsuch A number of previous studies have attempted to address the projects. financialaspectsofaphytoremediationproject.Lewandowskietal. Tosimplifythemodel,intangibleandindirecteconomicbene- [65] evaluated the economic value of combination of biomass fits,suchascostreductionsfromusingphytoremediationinplace production from cadmium contaminated land and the potential of more costly ex-situ clean-up technology and avoidance of Table4 Stochasticparametersofthemodelandtheirprobabilitydistributions. Symbol Parameters Grapha Min Mean Max 5% 95% Y P.vitattayield(kg/ha) 798 1353 1945 932 1789 H.annuusyield(kg/ha) 7814 9777 12994 8047 12200 B.coddiiyield(kg/ha) 9170 13473 20491 9775 18701 P.vitattaAsuptake(g/kg) 3.01 9.89 20.89 3.81 17.95 C H.annuusAsuptake(g/kg) 1.25 1.47 1.61 1.30 1.59 B.coddiiNiuptake(g/kg) 2.00 5.03 7.44 2.78 6.94 B.coddiiPtuptake(g/kg) 0.21(cid:3)10(cid:1)4 1.82(cid:3)10(cid:1)4 3.57(cid:3)10(cid:1)4 0.62(cid:3)10(cid:1)4 3.09(cid:3)10(cid:1)4 Cv RangeofHHVofwoodyBiomass(MJ/kg) 18.00 19.17 21.30 18.08 20.70 Ve Elec.FeedinTariff(£/kWh)b 0.0803 0.0810 0.0986 0.0830 0.0965 he Electricalefficiency(%) 27.1 33.7 39.4 29.0 38.0 hth Heatefficiency(%) 40.6 51.0 61.7 43.2 59.0 a Thegraphsshowthedistributionofprobabilityoftheinputdata,verticallengthofthebarindicatestheprobabilityofoccurrence. b Assumingadvancedthermochemicalbiomasstoenergytechnologyisused,andthereforereceiving2RenewableObligationCertificates(ROCs)/MWh.ValueofROCsvaries between£40e50.Sourceofdata:DepartmentofEnergy&ClimateChange,UK.http://chp.decc.gov.uk/cms/renewables-obligation-2/. 336 Y.Jiangetal./BiomassandBioenergy83(2015)328e339 disposalofbiomassarenotconsidered. Y¼Biomassyield(kgdryweightha(cid:1)1):Canrangefrom2000to A schematic overview of the main factors that influence the 20,000dependingonplants profitofanintegratedphytoremediationprojectisshowninFig.3. C¼Metalconcentrationinthebiomass(gkg(cid:1)1ondryweight Twodirectincomestreamsaretakenintoaccountinthemodel: basis) 1.)harvestedbiomassofwhichbiomasscalorificvalue(CV),elec- Cv¼Biomasscalorificvalue(CV)(MJkg(cid:1)1)(16.7e18.6MJkg(cid:1)1) tricity and thermal efficiency of the combined heat and power Vm¼Marketvalueofmetal(£Kg(cid:1)1) (CHP) unit, heat and electricity tariff are the determinants Ve¼ElectricityfeedingTariff(£/kWh) (Assumingadvancedgasificationtechnologyisusedtoproducefuel Vth¼HeatfeedingTariff(£/kWh) gasforasmallscale(50e1000KW)gasengineCHPunit).Currently, Rm¼Metalrecovery(%):Assuming100%here asaincentivetotherapidandsustaineddeploymentofrenewable he¼ElectricalefficiencyofaCHPunit energy, a feed-in tariffs (FITs) or similar schemes have been hth¼HeatefficiencyofaCHPunit(Generallyhth/he¼1.2e1.8) implementedin63jurisdictionsworldwidebytheregulators.This Es ¼ Cost of metal recovery per kg of dry biomass (£ kg(cid:1)1): schemes offer guaranteed prices for fixed periods of time for Estimatedat£0.4kg(cid:1)1frombiomassash(10%ofDMbiomass)by electricity/heatproducedfromrenewableenergysources[66].Asa smeltingaccordingtoGrayetal.[26]. result, this significantly reduces the uncertainties to the project Ep¼Costofgrowingplantsperhectare(£ha(cid:1)1) income by eliminating price fluctuation in energy market. 2.) Elemental recovery from biomass, of which market value of the Equation (1) attempts to capture the major determinants that elementisthedeterminant.Concomitantprocesscosts,i.e.costof affect gross margin of an integrated phytoremediation project. plantingandmaintainingthecropandcostofmetalrecoveringare Within the variables in Equation (1), Vth, Vm, Es and Ep are more deductedfromtheincome.Thereforethenetprofitmodelonthe deterministic and tend to be project specific. Once the project 1st harvest (per each hectare land) of an integrated phytor- location,scaleofoperation,localgovernmentincentivepoliciesare emediationprojectiscalculatedasfollowing: determined,thesevariableswillnotcontributesignificantlytothe financial risk of the project. To present a UK scenario, values of P¼Y(cid:3)C(cid:3)Vm(cid:3)Rmþ0:2778kWhMJ(cid:1)1(cid:3)Y(cid:3)Cv(cid:3)ðVe(cid:3)he thesevariablesusedinthisstudyareUKspecific(typicalvaluesthat þVth(cid:3)hthÞ(cid:1)0:1(cid:3)Y(cid:3)Es(cid:1)Ep ubesefodrefoarpcpalylcinuglatthioenmineththoidsdsetuscdryibaerdehliesrteediniannTyarbelaell3if)e. pHroowjeecvte,irt, (1) iscriticallyimportanttocollectthesedeterministicdataperproject inordertoobtainrealisticresults. Where: Fig.4. Outputoffinancialriskanalysisof2hypotheticalscenarioseusingPterisvittataandHelianthusannuusinintegratedphytoremediationprojectsonanarseniccontaminated site. Y.Jiangetal./BiomassandBioenergy83(2015)328e339 337 Othervariablessuchasbiomassyield(Y),metalconcentrationin theeconomicmotivationsneededtoestablishwiderapplicationof biomass (C), biomass calorific value (Cv), and electrical and heat thistechnology. efficiency(heandhth)oftheCHPunithaveawiderangeofreported Inthescenariousingthelowbiomassyieldhyperaccumulatorp. values as can be seen in the previous review. This causes uncer- vittatainanintegratedlandremediationprojecttorecoverarsenic tainty,andthusa‘risk’tothefinancialreturnoftheproject.Indeed, and produce energy, the probability distribution of the profit (P) therangeanddistributionofinputdataforthesestochasticvari- clearlysuggestsahighriskofloweconomicreturn.Inallpossible ablesdeterminethelevelofprofitthatcanbemadealongsidethe datacombinationssimulated,96%oftheoutcomesfailedtoachieve probabilitiesofachieving,orfailingtoachieveaprofit.Tounder- a positive margin and only 4% of outcomes achieve a limited standhowthesestochasticvariablesinfluencetheoutcomeofthe financial gain of £0e44.63 per ha (Fig. 4a). Among all stochastic economic model, a quantitative analysis based on Monte Carlo variables, biomass yield is the most significant variable affecting simulation method was carried out using risk analysis software themargin(Fig.4b).Thisisunderstandableasalargeproportionof @RISK(PalisadeCorp.Ithaca,NY,USA).Fourscenariosofdifferent incomeobtainedinthisscenarioisachievedfromenergygenerated target element and their corresponding accumulating plant (As/ frombiomass. P.Vitatta,As/H.annuus,Ni/B.coddiiandPt/B.coddii)werestudiedto Inadifferentscenario,P.vittataisreplacedwithahighbiomass compare the profitability of an integrated phytoremediation yield plant H. annuus. Although it has a lower accumulation ca- approachundereachscenario.Fromthecomprehensiveliterature pacity for arsenic, its high biomass energy value gives a signifi- reviewof(hyper)accumulatorsfortheelementsofinterestinthe cantlyimprovedfinancialreturn.Thereisahighcertainty(90%of previoussection,setsofdataforthestochasticvariableshavebeen simulated combinations) of achieving a margin of between compliedandtheirrangesandtriangularprobabilitydistributions £610e1434perhawiththehighestcalculatedmarginof£1730per usedforthesimulationareshowninTable4.Basedontheseinput ha(Fig.4c).Inbothscenarios,thebioaccumulationcapacityisless distributions,allvalidcombinationsofthevalueswerecalculated importantduetothelowmarketvalueofAs(Fig.4d).Thereforeit tosimulateallpossibleoutcomesofthemodel. canbeconcludedthatrecoveryoflowvaluearsenicisnotfinan- cially viable unless high value products can be subsequently 3.2. Riskmanagementoftheintegratedphytoremediationproject developed. This finding is consistent with previous work carried outbyGrayetal.[26]. Whilstphytoremediationisamaturetechnology,anintegrated Based on simulation results from these 2 scenarios, it can be approachincreasestheuncertaintyoftheoverallfinancialviability expected that the financial gain can be further improved if high oftheproject.Thereforeeconomicchallengesandrisksthatreside biomass producing plants with high accumulating capacity are withintheintegratedremediationhavetobeappraisedalongside usedinprojectstorecovermetalssuchasnickel. Fig.5. Outputsoffinancialriskanalysisof2hypotheticscenariosinanintegratedphytoremediationprojectusingBerkheycoddiiintorecoverNiandPt,respectively.