Air biomonitoring of heavy metals and polycyclic aromatic hydrocarbons near a cement plant

Air biomonitoring of heavy metals and polycyclic aromatic hydrocarbons near a cement plant

 AtmosphericPollutionResearch5(2014)262Ͳ269 Atm spheric Pollution  Research  Air biomonitoring of heavy metals and...

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Air biomonitoring of heavy metals and polycyclic aromatic hydrocarbons near a cement plant DanielaBaldantoni1,FlaviaDeNicola2,AnnaAlfani1 1

DipartimentodiChimicaeBiologia,UniversitàdegliStudidiSalerno,ViaGiovanniPaoloII,132– 84084Fisciano,SA,Italy DipartimentodiScienzeeTecnologie,UniversitàdegliStudidelSannio,ViaPort’Arsa,11–82100Benevento,Italy



Biomonitoringstudies,basedonpollutantaccumulationanalysesintreeleaves,allowevaluatingtheimpactcausedbyair– dispersedpollutantsonecosystems,providingusefuldata,complementarytothoseobtainedbyinstrumentalmonitoring. In particular, leaves of sclerophylls present morphological characteristics, such as the presence of hairs and of a tick cuticle,makingthemparticularlyusefulinbioaccumulationstudies.Thefirstaimofthisresearchwastocompareheavy metal(HM)andpolycyclicaromatichydrocarbon(PAH)leafaccumulationcapabilitiesoftwoMediterraneantreespecies. The second aim was to evaluate the impact of a cement plant and/or of other anthropogenic activities occurring in industrial and urban areas on HM and PAH depositions. For these purposes, holm oak (Quercus ilex L.) and olive (Olea europaeaL.)leavescollectedalongatransectindustrial–urban–remotesitesinsouthernItalywereemployed.Adifferent accumulationdegreewasobservedforthetwospecies.ForHMs,Q.ilexleaveshadthehighestconcentrations.Theresults showedthattheinfluenceofthecementplantemissionsonpollutantconcentrationswassubstantialintheareacloserto clinker production and storage  with the highest Pb, Ni, V, Cr, Fe, indeno(1,2,3–c,d)pyrene, benzo(g,h,i)perylene and benzo(a)anthracene leaf concentrations. However, Q. ilex leaves showed high HM and PAH concentrations also in the urbansite,inrelationtovehiculartrafficemissionsanddepositions.Thecomparisonoftheresultsofthepresentstudy withthosefromtheliteratureindicatesthattheoverallairqualityofthestudiedsitesisnotparticularlycompromised,also in proximity of the cement production. The use of holm oak should be preferred in biomonitoring due to its wider distributioncomparedtoO.europaea.



Flavia De Nicola

:+39Ͳ0824Ͳ305115 :+39Ͳ0824Ͳ305147

:[email protected] 

ArticleHistory: Received:28October2013 Revised:24December2013 Accepted:03January2014


1.Introduction  Heavy metals (HMs) and organic compounds, such as polycyclicaromatichydrocarbons(PAHs),aswellasdustandother pollutants, have been identified in the emissions from cement plants (Koren and Bisesi, 2003). The use of solid wastes, as supplementary fuel or as raw material substitute, and several processes associated with cement manufacturing result in high emissions of HMs. In spite of the fact that metals are frequently blocked within the clinker, some of them are volatilized and condenseonthedustparticles(Schuhmacheretal.,2002;Isikliet al.,2003;Isiklietal.,2006).EstimatedatmosphericemissionsofAs, Cd,Cr,NiandPbfromcementproductionwereof124,116,692, 769and892tons,respectivelyinEuropefortheyear2000(Pacyna etal.,2007).Al,Be,Cu,MnandZnhavealsobeendistinguishedin the emissions from cement plants (Schuhmacher et al., 2002). In addition,combustionprocessesandinparticularcementmanufacͲ turinghavebeenpointedoutasoneofthemostimportantsources of PAHs released into the atmosphere (Kaantee et al., 2004). However, the emissions of PAHs (quantity and type) linked to cementproductiondependonthefuel,themanufacturingprocess and the pollution control devices. The emissions can be transported through air mass movements, deposited at local and long–range, determining impacts and imbalances in the receiving environment. HMs and PAHs are toxic pollutants altering ecosystems. They are hazardous for human beings as particles to whichthesepollutantsareassociatedcanbeinhaledandingested (Domingo,1994;Chang,1996;IARC,2013).  Studiesonthedegreeofenvironmentalcontaminationdueto

cementplantactivitiesandthesubsequentimpactsonecosystem health (Orecchio, 2010) are scarce. Some studies highlighted the negativeimpactofcementdustonsoilcommunityandtheeffect of the altered soil composition on vegetation growth (Ade– AdemiluaandUmebese,2007).  Toevaluatetheenvironmentalqualityandtheimpactcaused by air–dispersed pollutants on ecosystems, treeleaveshave been widely and effectively employed in biomonitoring studies, as alternative to instrumental monitoring. Although a quantitative relationship between air and plant concentrations of pollutants is not yet established, leaf content of pollutants mirrors their air concentrations (Alfani et al., 2000; De Nicola et al., 2011), providing time–averaged information on air contamination trends (Kardel et al., 2011). Moreover, biomonitoring can provide high spatial resolution because plants are widely distributed and relatively inexpensive. Tree leaves in particular are efficient in trapping gaseous and particulate air pollutants depending on leaf characteristics.Morphologicalandphysiologicalleafcharacteristics affectscavengingefficiencyofairpollutants(Howsametal.,2000). Leaves of several evergreen and deciduous tree species may be usedasbiomonitorsforbothinorganicandorganicpollutants(De Nicolaetal.,2011;Tomasevicetal.,2011).  Themaingoalsofthepresentstudywere(i)tocompareHM andPAHleafaccumulationcapabilitiesoftwoMediterraneantree species, namely holm oak (Quercus ilex L.) and olive (Olea europaea L.), collected along a transect industrial–urban–remote areas; (ii) to evaluate the impact of a cement plant and/or other anthropogenicactivitiesoccurringinindustrialandurbanareason


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 HM and PAH depositions at local scale. The two selected species arewidelyspreadinMediterraneanregions.Q.ilexrepresentsthe potential natural vegetation community in remote areas, and in urbanareasitisusedasornamentalplant.O.europaeaispresent asawildanddomestictreeinanthropogenicandruralareas.Both species can have leaves up to 3–4 years old and they display morphologicaladaptivecharacteristics(xeromorphism)inresponse to environmental constraints under Mediterranean climate, such asthepresenceofhairsandatickcuticle.Thesecharacteristicsare particularly useful in biomonitoring: the lifespan facilitates pollutantaccumulationoveralongperiod,thestar–liketrichomes on abaxial surface enhance the scavenging and retention of airborne particulate, whereas the cuticular waxes promote the accumulation of lipophilic organic pollutants (De Nicola et al., 2005,Sawidisetal.,2012).  

2.MaterialsandMethods  2.1.Sampling  Sampling was carried out in May 2008 inside the area of the ItalcementiGroupcementplant(A,B,C,andD)andinotherfour sites, in particular in urban (E), industrial quarry (F), rural (G) and remote (H) areas, all located in Salerno province, Campania, southernItaly(Figure1,Table1).Themainwinddirectionsinthe studied area are reported in Figure 2 (Campania Region, 2010). Within the area of the cement plant, sites A and B were located along the main road access, site C near the clinker processing (milling,kilnandstoragepoint),siteDneartruckstationingpoint. Aplanofthecementplantreportingtheenergyandheatflows,as well as gaseous and particulate emissions, is shown in Figure S1 (seetheSupportingMaterial,SM).



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 Table1.Name,latitude,longitudeandaltitude(ma.s.l.)ofthesamplingsites(Salerno,southernItaly).Thebiomonitorspeciesfoundineachsitehave alsobeenreported Site










BiomonitorSpecies Q.ilex


















Q.ilexͲO.europaea Q.ilex
























Figure2.Winddirectionsinthestudiedarea,atdifferentheightsfromthe st st ground,intheperiodof1 January2004Ͳ1 January2009(from CampaniaRegion,2010).

 The Italcementi Group cement plant, built in 1992 to replace the old plant of Salerno, produces cement from extraction and preparation of raw materials (clay, limestone and gypsum), their grinding and subsequent burning at 1450°C. It produces on average400000 Mgofclinkerand700000Mgofcementperyear (Italcementi,2007).  At each sampling site, healthy one–year old leaves of Q. ilex and, if present (see Table 1), of O. europaea were collected from the outer part of the canopy of 3–5 trees, at about 2–4 m above the ground, and pooled in a homogeneous sample. Leaves were picked up taking care to minimize the contact with hand and analyzedwithoutwashing.Theresultswerereportedasaverageof threereplicatesonadryweightbasis.  2.2.Laboratoryanalyses  Leaves from each site were characterized (Table 2) for their watercontentviagravimetricmethodafteroven–drying(75°C)to constant weight, and for C and N concentrations by a CHNS–O Analyzer (Thermo, Flash EA 1112). The leaf samples were oven– dried at 75°C for element analyses or stored at –20°C in polyethylene bags for PAH analyses. Briefly, leaf HM concentraͲ tions were measured by AAS (PerkinElmer, AAnalyst 100) via graphitefurnace(Cd,Cr,Cu,Ni,PbandV)orviaflame(Fe,Mnand Zn), after acidic mineralization of the samples in a micro–wave oven(Milestone,Ethos),asreportedinBaldantonietal.(2009).To ascertain the accuracy of the method employed, a concurrent analysis of standard reference material (1575a Pine Needles –

NIST, 2004) was carried out. Recoveries ranged from 86 to 99%, and metal concentrations were corrected for the recoveries accordingly. For PAH analyses, leaf samples were extracted by sonication (Misonix, XL2020) in a dichloromethane–acetone mixture.Theextractswererotaryevaporated,purifiedandgently dried under a nitrogen stream. Consecutively, the dried residues were added with internal standards and brought to the final volume with cyclohexane. The PAH concentrations were determined by GC–MSD (HP5890–HP5971) with the internal standard method. To evaluate the extraction efficiency, each samplewasspikedbeforetheextractionwithamixofdeuterated PAHs (acenaphthene–D10, phenanthrene–D10, chrysene–D10 and perylene–D12 at known concentrations). Recoveries were about 75–92%,andPAHconcentrationswerecorrectedfortherecoveries accordingly. PAHs were reported either as the sum of the concentrations of all compounds (total) and divided according to their molecular weight in low (LMW): acenaphthylene (Acy), acenaphthene (Ace), fluorene (Flu); medium (MMW): phenanthrene(Phen),anthracene(Ant),fluoranthene(Flt),pyrene (Pyr), benzo[a]anthracene (B[a]A), chrysene (Chry); high (HMW): benzo[b+k+j]fluoranthene (B[bkj]F), benzo[e]pyrene (B[e]P), benzo[a]pyrene (B[a]P), perylene (Per), indeno[1,2,3–c,d]pyrene (IP), dibenzo[a,h]anthracene (DB[ah]A), benzo[g,h,i]perylene (B[ghi]P), dibenzo[a,e]pyrene (DB[ae]P), coronene (Cor), dibenzo[a,h]pyrene (DB[ah]P), dibenzo[a,i]pyrene (DB[ai]P), dibenzo[a,l]pyrene (DB[al]P). Further details on PAH analyses, together with the features and operating conditions of GC–MS system,werereportedinDeNicolaetal.(2013a).  Table 2. Mean values of water content (% f.w.) and mean values ± s.e. of carbon and nitrogen concentrations (% d.w.) in leaves of Q. ilex and O. europaea collected at cement plant (AͲD), urban (E), industrial quarry (F), rural(G)andremote(H)sites Site A B C D E F G H


Water content






O.europaea Q.ilex































O.europaea Q.ilex O.europaea Q.ilex













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 2.3.Statisticalanalyses  To explore the separation among the sites in relation to the relative HM and PAH distributions, separately for Q. ilex and O. europaea leaves, the Correspondence Analysis (CA) was applied. The analysis was performed with the R 3.0.2 programming language(RCoreTeam,2013),usingthefunctionsofthe"vegan" package(Oksanenetal.,2013).  ThesigniĮcanceofdifferencesinHMandPAHconcentrations among the sites was separately analyzed for Q. ilex and O. europaea leaves by one–way analysis of variance (ANOVA) or by Kruskal–Wallis rank sum test, according to the distribution of the data, followed by the Tukey post hoc test (ɲ=0.05). Normality of the residuals and homoscedasticity were assessed by the Kolmogorov–Smirnov and the Breuch–Pagan tests, respectively. The analyses were carried out with the SigmaPlot 11.0 (Systat Software,Inc)softwarepackage. 

2007;DeNicolaetal.,2013b).HMsemittedinatmospherecanbe intercepted by tree leaves, remaining on the leaf surface or entering the leaf tissues, although a selective metal uptake by roots can also affect metal contents in leaf tissues (Maisto et al., 2013). The main uptake pathways for PAHs are reported to be gaseous and particle–bound deposition via foliage. PAHs could migrate after deposition on the leaf surface into cuticular waxes (De Nicola et al., 2008) whereas the contribution of the root uptake to PAH leaf concentrations is negligible (some authors reported the exception of two–ring PAHs, see Yin et al., 2011). PreviousstudiesreportedthatunwashedQ.ilexleavesmorethan washedonesclearlyspotlightspatialaircontaminationtrends(De Nicolaetal.,2008)andbetterhighlighttheeffectsofdryandwet depositions. 

3.Results  2 CA, an ordination technique based on the ʖ  distance (Legendre and Legendre, 1998), allowed differentiating sampling sites in relation to relative leaf accumulation of single HMs and PAHs.WecarriedoutthisordinationseparatelyonthedataofQ. ilex and O. europaea leaves and the results were reported in Figure3. The analysis of Q. ilex leaves highlighted that the site C inside the cement plant was characterized by significantly higher concentrations of Pb, Ni, V, Cr and Fe (Figures 3 and 4), and by higher concentrations of indeno(1,2,3–c,d)pyrene, benzo[g,h,i] perylene and benzo[a]anthracene (Figure 3). In the same site, O. europaealeavesshowedsignificantlyhigherconcentrationsofPb, V and Zn (Figures3 and 4), and higher concentrations of anthracene (Figure3). The other sites inside the cement plant (A, B, D) showed similar values for both HM and PAH concentrations (Figures4 and 5). At the urban site (E) Q. ilex leaves showed significantlyhigherNi,Fe,CrandPbconcentrationsrespecttothe sitesinsidethecementplantarea,exceptforthesiteC(Figure4). At the site E, Q. ilex leaves showed total PAH concentrations significantlyhigherthaninsidethecementplant(A–Dsites).Atthe industrial quarry (F) the acenaphthylene concentration (Figure3) was responsible for the highest total PAH concentrations (Figure5). To different extent, an accumulation in both holm oak and olive leaves from industrial–urban sites respect to rural– remote ones was always detected for both HMs and PAHs (Figures4and5).  Holm oak and olive leaves showed different accumulation degrees. Q. ilex leaves showed for Cr, Fe, Mn, Ni, Pb and V concentrations one order of magnitude higher than O. europaea leaves (Figure 4). This held true also for Cd, for which Q. ilex concentrationswere0.006,0.845and0.001μgg–1d.w.atthesites B, C and F, respectively, in comparison with 0.018μgg–1 d.w. measured in O. europaea at the site C (in all the other sites concentrations were below the detection limit, for both the species,andthusCdhasnotbeenreportedinthefigure).Holmoak and olive leaves showed similar Zn concentrations, whereas olive leaves highlighted higher Cu concentrations. Leaves from the two species showed similar total PAH concentrations (Figure5), although the percentage contribution of different molecular weight PAHs differed between the two species, and often among the sites (Figure 6). In Q. ilex leaves MMW PAHs were most abundant at all the sites, with the exception of E and F, in which LMW PAHs prevailed (Figure 6). On the contrary, in O. europaea leavesHMWPAHsweremostabundant,withtheonlyexceptionof thesiteG,inwhichMMWPAHsprevailed(Figure6). 

4.Discussion  Itiswidelyrecognizedthatleavesofselectedtreespeciescan act as monitors of global and local air contamination (Smodis,

Figure3.CorrespondenceAnalysis(CA)forQ.ilex(upper)andO.europea (below)leaves.Thecentroidofeachsite,incapitalboldletters,isalso reported.TheabbreviationsofPAHsarereportedinthetext.

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 Figure4.MeanHMconcentrations±SDinleafsamplesofQ.ilexandO.europaeacollectedatcementplant(AͲD),urban(E), industrialquarry(F),rural(G)andremote(H)sites.InA,E,FandHonlyQ.ilexispresent(seealsoTable1). Asteriskindicatesthevaluebelowthelimitofdetection.

Figure5.MeanPAHconcentrations±SDinleafsamplesofQ.ilexandO. europaeacollectedatcementplant(AͲD),urban(E),industrialquarry(F), rural(G)andremote(H)sites.InA,E,FandHonlyQ.ilexispresent(see alsoTable1).

Comparingthepollutantconcentrationsinholmoakandolive leavesfromanthropogenicandnaturalareas,ourfindingsshowed different accumulation degrees, above all in respect to HMs. In fact, whereas Q. ilex showed concentrations higher than O. europaea for most of the metals analyzed, leaves of the two species showed similar total PAH concentrations, even if differences in accumulation of low, medium and high molecular weight PAHs were detected. The higher leaf HM accumulation capability of Q. ilex compared  to O. europaea have already been reportedpreviously(Madejonetal.,2006;Dominguezetal.,2008) together with the differences in PAH accumulation capability, in relation to molecular weights, depending on morphology and chemicalcompositionofleavesofthetwospecies.Leafroughness and exposed surface area, tricome structure and density (Karabourniotis et al., 1998), as well as cuticle thickness, density and composition (Schreiber and Riederer, 1996; Martins et al., 1999;Liakopoulosetal.,2001;Bacelaretal.,2004)mayinfluence the capture of aerial dust and the accumulation of both HMs (Madejon et al., 2006) and particle–bound PAHs (Howsam et al., 2000). These characteristics are responsible for the observed differencesbetweenthetwospeciesinthepercentageofdifferent

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 molecular weight PAHs. The greater capability of olive than holm oak leaves to retain small particles (Federica Fantozzi, personal communication),towhichHMWPAHsaremainlylinked(Wingfors et al., 2001; Park and Kim, 2005) explains the higher HMW PAH accumulation in O. europaea than in Q. ilex. The PAHs present in gaseousphase,i.e.thosewithlowernumberrings,candiffuseinto the leaves through cuticle and via stomata, migrate into intercellular air spaces and be stored in lipophilic compounds or compartments, such as essential oils, resins, surface lipids, cuticular waxes (Collins et al., 2006). Variability in PAH accumuͲ lationsamongspecieshasbeenreportedalsoaffectedbycuticular permeability to organic chemicals (Buckley, 1982; Schreiber and Riederer, 1996). When gaseous uptake is the main uptake pathway, not only the content but also the chemical composition oflipidsitisnoteworthytoexplaininterspecificdifferencesinPAH concentrations. Being the gas exchange also involved in gaseous PAH uptake, not only leaf chemical composition but also plant physiologyplaysaroleintheuptakeofthesePAHs,aspreviously reported (De Nicola et al., 2008). However, it is important to remember that the uptake of these PAHs by leaves can be kinetically limited if the leaves will not come into contact with a sufficient air volume to became saturated with these compounds (McLachlan, 1999). So, the surface area of leaves became of primary importance for chemical compounds that not reach the equilibriumpartitioning. 

Figure6.Meanconcentrations±SDoflow(LMW),medium(MMW)and high(HMW)molecularweightPAHsinleafsamplesofQ.ilexandO. europaeacollectedatcementplant(AͲD),urban(E),industrialquarry(F), rural(G)andremote(H)sites.InA,E,FandHonlyQ.ilexispresent(see alsoTable1).

 Apart from the different leaf accumulation degrees between the two species, the impact of the emissions from the cement plant,aswellasaspatialtrendofHMsandPAHsalongatransect fromindustrial–urbantoremoteareaswerehighlighted.Insidethe cement plant area, the site C was characterized by the highest

concentrations of several HMs, whereas the other sites were less ornotaffected.Comparingleafmetalconcentrationsmeasuredin holm oak with values reported as typical for this species by Bargagli (1998), very high concentrations of all metals, except Zn andMn,resultedatthesiteCinsidethecementplant.Inthissite, also olive leaves showed higher Cu and Zn concentrations when comparedtothosemeasuredinleavescollectedataspillaffected site (Dominguez et al., 2008). The site C was close to the area where the processing of raw material occurs, and to the kiln that produces particulate emissions (see the SM). Even if dust generated from cement plants is termed fugitive and it is discharged into the atmosphere in a non–conĮned Ňow (Abdul– Wahab,2006),theeffectsofdustdepositionwereseenonlyinthe area closer to the kiln. The production of clinker requires several steps, from crushing and milling of raw materials to cooking at temperatures over 1400°C, to subsequently fine milling, each associated with typical emissions. However, although in the Italcementi Group cement plant a particular fuel characterized by lowparticulateemissionsisused,fueloilcannotbeexcludedasa metalsource.Holmoakleavescollectedinthecementplantarea (including site C) showed HM concentrations often lower than thosepreviouslydetectedinotherCampaniaurbansites(Alfaniet al.,2000;Maistoetal.,2013),indicatinganoverallairqualitythat is not degraded substantially. Also referring to highest Cu concentrationinoliveleavesatthesiteBinsidethecementplant area,itwaslikelyattributabletocoppersulfatetreatmentsapplied tothetrees,asobservedatthesamplingtime,ratherthanthatto atmosphericdeposition.  High HM concentrations referred to Q. ilex chemical fingerprint (Bargagli, 1998), particularly of Fe, Cr and Cu, were measuredintheurbansiteE,asaconsequenceofvehiculartraffic emissions (see for example Alfani et al., 2000). Leaf metal concentrations measured at this site were comparable to those previouslyreportedforunwashedleavesofurbanareas,exceptfor Cr that showed two–fold higher values at the site E than those previouslyreported(DeNicolaetal.2008).  RegardingPAHs,althoughacenaphthylene,acenaphtheneand anthraceneareconsideredindicatoryofcementplants(Yangetal., 1998), leaf concentrations of these 3–ring PAHs in the cement plant area were always lower than those detected in the urban areaE,highlightingamajorinfluenceofvehiculartrafficemissions (De Nicola et al., 2011). Moreover, total PAH concentrations measured in holm oak leaves collected in the cement plant area, includingsiteC,werealwayslowerthanthosepreviouslydetected in other Campania industrial–urban sites (De Nicola et al., 2011). Although the properties of olive leaves make them a potentially good accumulator of PAHs, as well as yet proved for POPs (Sofuogluetal.,2013),andaspreviouslyestablishedbycorrelation betweenPAHconcentrationsintheparticulatematterandinolive leaves (Librando et al., 2002), the lack of olive trees in urban– industrial–remote areas did not allow to test their feasibility to highlightairPAHspatialtrends.  Notwithstanding the similar pollutant trends among sites between the two species, the wider distribution of Q. ilex in respecttoO.europaeasuggeststhatholmoakshouldbepreferred in biomonitoring studies in the Mediterranean area. In fact, holm oak represents the climax species in the Mediterranean natural woodlands and is widely represented also in urban parks, along urban streets and in industrial surroundings, whereas, olive is mainly associated to agricultural lands. Information derived from the biomonitoring of industrial emissions could be employed to steer an environmental sustainable management of industrial processesatlocalscale. 

Acknowledgments  ItalcementiGroupcementplantofSalerno(Italy)isgratefully acknowledged to allow sampling. We thank Dr. Federica Fantozzi

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 (UniversityofSiena)fortheusefuldatadiscussionandDr.Ludovica Sessa (University of Salerno) for the support in laboratory. This work was financially supported by University of Salerno (FARB 2007). 

SupportingMaterialAvailable  Plan of the Italcementi Group cement plant of Salerno (Italy) reportingtheenergy(E)andheat(H)flows,aswellasgaseous(G) and particulate (P) emissions (Figure S1). This information is available free of charge via the internet at http://www. 

References  Abdul–Wahab, S.A., 2006. Impact of fugitive dust emissions from cement plantsonnearbycommunities.EcologicalModelling195,338–348. Ade–Ademilua,O.E.,Umebese,C.E.,2007.ThegrowthofPhaseolusvulgaris L. cv. Ife Brown (Leguminosae) in a cement site rich in heavy metals. PakistanJournalofBiologicalSciences10,182–185. Alfani, A., Baldantoni, D., Maisto, G., Bartoli, G., Virzo De Santo, A., 2000. TemporalandspatialvariationinC,N,Sandtraceelementcontentsin the leaves of Quercus ilex within the urban area of Naples. EnvironmentalPollution109,119–129. Bacelar,E.A.,Correia,C.M.,Moutinho–Pereira,J.M.,Goncalves,B.C.,Lopes, J.I.,Torres–Pereira,J.M.G.,2004.Sclerophyllyandleafanatomicaltraits of five field–grown olive cultivars growing under drought conditions. TreePhysiology24,233–239. Baldantoni, D., Ligrone, R., Alfani, A., 2009. Macro– and trace–element concentrationsinleavesandrootsofPhragmitesaustralisinavolcanic lake in Southern Italy. Journal of Geochemical Exploration 101, 166– 174. Bargagli,R.,1998.TraceElementsinTerrestrialPlants.AnEcophysiological ApproachtoBiomonitoringandBiorecovery,Springer–Verlag,Berlin. Buckley,E.H.,1982.Accumulationofairbornepolychlorinated–biphenylsin foliage.Science216,520–522. Campania Region, 2010. comunicati/pdf/AIB_2010.pdf,accessedinJanuary2014. Chang,L.W.,1996.ToxicologyofMetals,CRCLewisPublishers,BocaRaton, FL,USA. Collins, C., Fryer, M., Grosso, A., 2006. Plant uptake of non–ionic organic chemicals.EnvironmentalScience&Technology40,45–52. DeNicola,F.,Spagnuolo,V.,Baldantoni,D.,Sessa,L.,Alfani,A.,Bargagli,R., Monaci, F., Terracciano, S., Giordano, S., 2013a. Improved biomonitoringofairbornecontaminantsbycombineduseofholmoak leavesandepiphyticmoss.Chemosphere92,1224–1230. DeNicola,F.,Murena,F.,Costagliola,M.A.,Alfani,A.,Baldantoni,D.,Prati, M.V., Sessa, L., Spagnuolo, V., Giordano, S., 2013b. A multi–approach monitoring of particulate matter, metals and PAHs in an urban street canyon.EnvironmentalScienceandPollutionResearch20,4969–4979.

Howsam,M.,Jones,K.C.,Ineson,P.,2000.PAHsassociatedwiththeleaves of three deciduous tree species. I – Concentrations and profiles. EnvironmentalPollution108,413–424. IARC (International Agency for Research on Cancer), 2013., accessed in October2013. Isikli,B.,Demir,T.A.,Akar,T.,Berber,A.,Urer,S.M.,Kalyoncu,C.,Canbek, M.,2006.Cadmiumexposurefromthecementdustemissions:Afield studyinaruralresidence.Chemosphere63,1546–1552. Isikli, B., Demir, T.A., Urer, S.M., Berber, A., Akar, T., Kalyoncu, C., 2003. Effects of chromium exposure from a cement factory. Environmental Research91,113–118. Italcementi,2007.,accessedinJanuary2014. Kaantee, U., Zevenhoven, R., Backman, R., Hupa, M., 2004. Cement manufacturing using alternative fuels and the advantages of process modelling.FuelProcessingTechnology85,293–301. Karabourniotis, G., Kofidis, G., Fasseas, C., Liakoura, V., Drossopoulos, I., 1998.PolyphenoldepositioninleafhairsofOleaeuropaea(Oleaceae) and Quercus ilex (Fagaceae). American Journal of Botany 85, 1007– 1012. Kardel, F., Wuyts, K., Maher, B.A., Hansard, R., Samson, R., 2011. Leaf saturation isothermal remanent magnetization (SIRM) as a proxy for particulatemattermonitoring:Inter–speciesdifferencesandin–season variation.AtmosphericEnvironment45,5164–5171. Koren, H., Bisesi, M., 2003. Handbook of Environmental Health. Pollutant InteractionsinAir,Water,andSoil,Volume2,Fourthedition,CRCLewis Publishers,BocaRaton,FL,USA. Legendre,P.,LegendreL.,1998.NumericalEcology,SecondEnglishedition, Elsevier,Amsterdam. Liakopoulos, G., Stavrianakou, S., Karabourniotis, G., 2001. Analysis of epicuticular phenolics of Prunus persica and Olea europaea leaves: EvidenceforthechemicaloriginoftheUV–inducedbluefluorescence ofstomata.AnnalsofBotany87,641–648. Librando,V.,Perrini,G.,Tomasello,M.,2002.Biomonitoringofatmospheric PAHs by evergreen plants: Correlations and applicability. Polycyclic AromaticCompounds22,549–559. Madejon, P., Maranon, T., Murillo, J.M., 2006. Biomonitoring of trace elements in the leaves and fruits of wild olive and holm oak trees. ScienceoftheTotalEnvironment355,187–203. Maisto,G.,Baldantoni,D.,DeMarco,A.,Alfani,A.,VirzoDeSanto,A.,2013. RangesofnutrientconcentrationsinQuercusilexleavesatnaturaland urbansites.JournalofPlantNutritionandSoilScience176,801–808. Martins, C.M.C., Mesquita, S.M.M., Vaz, W.L.C., 1999. Cuticular waxes of the holm (Quercus ilex L. subsp. ballota (desf.) samp.) and cork (Q. suberL.)oaks.PhytochemicalAnalysis10,1–5. McLachlan,M.S.,1999.Frameworkfortheinterpretationofmeasurements ofSOCsinplants.EnvironmentalScience&Technology33,1799–1804.

De Nicola, F., Lancellotti, C., Prati, M.V., Maisto, G., Alfani, A., 2011. BiomonitoringofPAHsbyusingQuercusilexleaves:Sourcediagnostic andtoxicityassessment.AtmosphericEnvironment45,1428–1433.

NIST(NationalInstituteofStandardsandTechnology),2004.Certificationof NIST Standard Reference Material 1575a Pine Needles and Results of anInternationalLaboratoryComparison,NISTSpecialPublication260– 156,–156.pdf, accessed in May2013.

DeNicola,F.,Maisto,G.,Prati,M.V.,Alfani,A.,2008.Leafaccumulationof trace elements and polycyclic aromatic hydrocarbons (PAHs) in QuercusilexL.EnvironmentalPollution153,376–383.

Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Wagner, H., 2013. Vegan:CommunityEcologyPackage,Rpackageversion2.0–8.

DeNicola,F.,Maisto,G.,Prati,M.V.,Alfani,A.,2005.Temporalvariationsin PAH concentrations in Quercus ilex L. (holm oak) leaves in an urban area.Chemosphere61,432–440.

Orecchio,S.,2010.Assessmentofpolycyclicaromatichydrocarbons(PAHs) insoilofaNaturalReserve(IsoladelleFemmine)(Italy)locatedinfront of a plant for the production of cement. Journal of Hazardous Materials173,358–368.

Domingo,J.L.,1994.Metal–induceddevelopmentaltoxicityinmammals–a review.JournalofToxicologyandEnvironmentalHealth42,123–141. Dominguez, M.T., Maranon, T., Murillo, J.M., Schulin, R., Robinson, B.H., 2008. Trace element accumulation in woody plants of the Guadiamar Valley, SW Spain: A large–scale phytomanagement case study. EnvironmentalPollution152,50–59.

Pacyna,E.G.,Pacyna,J.M.,Fudala,J.,Strzelecka–Jastrzab,E.,Hlawiczka,S., Panasiuk, D., Nitter, S., Pregger, T., Pfeiffer, H., Friedrich, R., 2007. Current and future emissions of selected heavy metals to the atmosphere from anthropogenic sources in Europe. Atmospheric Environment41,8557–8566.

Baldantoni et al. – Atmospheric Pollution Research (APR)


 Park,S.S.,Kim,Y.I.,2005.Sourcecontributiontofineparticulatematterin anurbanatmosphere.Chemosphere59,217–226. R Core Team, 2013. R: A Language and Environment for Statistical Computing.RFoundationforStatisticalComputing,Vienna,Austria. Sawidis, T., Krystallidis, P., Veros, D., Chettri, M., 2012. A study of air pollution with heavy metals in Athens city and Attica basin using evergreen trees as biological indicators. Biological Trace Element Research148,396–408. Schreiber, L., Riederer, M., 1996. Ecophysiology of cuticular transpiration: Comparative investigation of cuticular water permeability of plant speciesfromdifferenthabitats.Oecologia107,426–432. Schuhmacher,M.,Bocio,A.,Agramunt,M.C.,Domingo,J.L.,deKok,H.A.M., 2002. PCDD/F and metal concentrations in soil and herbage samples collectedinthevicinityofacementplant.Chemosphere48,209–217.

Sofuoglu,S.C.,Yayla,B.,Kavcar,P.,Ates,D.,Turgut,C.,Sofuoglu,A.,2013. Olive tree, Olea europaea L., leaves as a bioindicator of atmospheric PCB contamination. Environmental Science and Pollution Research 20, 6178–6183. Tomasevic, M., Anicic, M., Jovanovic, L., Peric–Grujic, A., Ristic, M., 2011. Deciduoustreeleavesintraceelementsbiomonitoring:Acontribution tomethodology.EcologicalIndicators11,1689–1695. Wingfors, H., Sjodin, A., Haglund, P., Brorstrom–Lunden, E., 2001. Characterisation and determination of profiles of polycyclic aromatic hydrocarbons in a traffic tunnel in Gothenburg, Sweden. Atmospheric Environment35,6361–6369. Yang,H.H.,Lee,W.J.,Chen,S.J.,Lai,S.O.,1998.PAHemissionfromvarious industrialstacks.JournalofHazardousMaterials60,159–174. Yin, H., Tan, Q., Chen, Y., Lv, G.B., Hou, X.D., 2011. Polycyclic aromatic hydrocarbons (PAHs) pollution recorded in annual rings of gingko (GingkobilobaL.):DeterminationofPAHsbyGC/MSafteraccelerated solventextraction.MicrochemicalJournal97,138–143.

Smodis, B., 2007. Investigation of trace element atmospheric pollution by nuclearanalyticaltechniquesataglobalscale:Harmonisedapproaches supported by the IAEA. Journal of Environmental Management 85, 121–128.