Potentially toxic element gradients in remote, residential, urban and industrial areas, as highlighted by the analysis of Quercus ilex leaves

Urban Forestry & Urban Greening 47 (2020) 126522

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Original article

Potentially toxic element gradients in remote, residential, urban and industrial areas, as highlighted by the analysis of Quercus ilex leaves

T

Daniela Baldantonia,*, Flavia De Nicolab, Anna Alfania a b

Dipartimento di Chimica e Biologia “Adolfo Zambelli”, Università degli Studi di Salerno, Via Giovanni Paolo II, 132 - 84084 Fisciano (SA), Italy Dipartimento di Scienze e Tecnologie, Università degli Studi del Sannio, Via F. De Sanctis, 82100 Benevento, Italy

A R T I C LE I N FO

A B S T R A C T

Handling Editor: A. Alessio Fini

Reconstructing spatial and temporal pollution gradients in natural and anthropogenic areas is of paramount importance to undertake proper mitigation strategies. To this end, air biomonitoring based on chemical analysis of selected bioaccumulators, provides useful information not only on the pollutant concentration gradients, but also on their possible effects on biota and ecosystems. The analysis of 18 potentially toxic elements (PTEs), namely macronutrients (Ca, K, Mg, P, S), micronutrients (Co, Cr, Cu, Fe, Mn, Na, Ni, V, Zn) and non-essential elements (Al, As, Cd, Pb), in Quercus ilex leaves collected from 26 sites belonging to remote, residential, urban and industrial areas of Salerno, in the Mediterranean area, provided accurate information on spatial and temporal air pollution gradients, as well as on the plant nutritional status within the whole area. Despite the adequate nutritional status of plants in all the site typologies, several criticalities were highlighted. Specifically, on a natural background contamination by Na (due to the sea proximity), Al and V (due to the lithological characteristics) of the whole area, anthropogenic activities were responsible for relatively high concentrations of selected PTEs in the different site typologies. Remote sites were affected by high Cd concentrations, due to the transport of fine particulate from urban or industrial areas. Urban (and to a lesser extent residential) sites were affected by high concentrations of most PTEs, mainly released by diffuse sources, such as vehicular traffic. Exceedingly high concentrations of As, Mn, Ni and Pb were observed in industrial sites, in relation to local and specific emissions. Anyway, an overall decrease, consistent with the general temporal trends observed in Europe in the last years, was observed in several PTE concentrations for all the site typologies.

Keywords: Biomonitoring Holm oak Mediterranean area Pollution gradients PTE accumulation

1. Introduction Potentially toxic elements (PTEs) are chemical elements of ensvironmental concern in relation to their persistence in both biotic and abiotic compartments (Boente et al., 2017; Alexakis et al., 2009). Although these elements naturally occur (Antoniadis et al., 2017), elevated concentrations of PTEs are usually linked to anthropogenic activities, particularly to vehicular (Keshavarzi et al., 2018) and industrial (Antoniadis et al., 2017) emissions. Since they have adverse effects on plants, animals and ecosystems, monitoring campaigns of PTE concentrations in soil, air and water compartments are needed, in order to carry out proper mitigation and remediation strategies. Despite several advantages, instrumental monitoring of a high number of PTEs has considerable limitations in terms of both temporal and spatial resolution, allowing only a coarse reconstruction of pollutant dynamics (Allan et al., 2006). Indeed, the high cost associated to

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the instrumental monitoring (Norouzi et al., 2015) usually imposes a trade-off between temporal and spatial sampling densities, often determining low sampling frequencies and/or low spatial sampling densities, unsuitable to reconstruct accurate PTE concentration gradients (Allan et al., 2006). In addition, data obtained from instrumental monitoring do not provide information on the actual PTE availabilities for biota (Allan et al., 2006; Baldantoni et al., 2018). Biomonitoring of PTEs, directly measuring their concentrations in selected bioaccumulators, is not only a cheap and accurate method to derive spatial concentration gradients, but also the unique way to evaluate the effects on organisms and higher organization levels, as well as the possible PTE transfer through food webs (Markert et al., 2003). For these reasons, biomonitoring of PTEs has been widely applied as a complementary method to instrumental monitoring (Markert et al., 2003; Tomašević et al., 2011). Urban trees, not only can mitigate the effects of heat and drought in

Corresponding author. E-mail addresses: [email protected] (D. Baldantoni), [email protected] (F. De Nicola), [email protected] (A. Alfani).

https://doi.org/10.1016/j.ufug.2019.126522 Received 26 May 2019; Received in revised form 23 September 2019; Accepted 4 November 2019 Available online 05 November 2019 1618-8667/ © 2019 Elsevier GmbH. All rights reserved.

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Fig. 1. Map of the 26 sampling sites along the Salerno municipality (green: remote areas, yellow: residential areas, red: urban areas, purple: industrial areas); background tiles from Bing maps. For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.

pressure: remote, residential, urban and industrial areas. The detection of spatial contamination gradients by leaf analyses can be used by planners to set-up an effective monitoring net in strategic locations of an urban area. The possibility to reconstruct, by biomonitoring, temporal patterns in pollutant concentrations overcomes the difficulty in monitoring environmental disturbance over long-time. In addition, quantifying the accumulation of PTEs by leaves can be important in planning strategies of greening management in urban and industrial areas, using trees able to capture pollutants carried by air particulate and decreasing human exposure to anthropogenic pollutants.

the cities (Brown et al., 2015), but can also provide air purification, through removal and fixation of pollutants in leaves (De Nicola et al., 2017a), and environmental quality assessment (Baldantoni et al., 2014). In particular, leaves of several tree species, either evergreen or deciduous, have been studied in the last decades to validate their use in deriving PTE concentration gradients in areas affected by different anthropogenic activities (Tomašević et al., 2011; De Nicola et al., 2017b). In addition, in terrestrial ecosystems, leaf PTE concentrations, reflecting both air PTE depositions and soil-plant PTE translocations (Maisto et al., 2013), provide an accurate overview of the quality of the study area. Holm oak (Quercus ilex L.) leaves have been effectively employed in biomonitoring of air and soil quality in Mediterranean area (Alfani et al., 2000; Madejón et al., 2006; De Nicola et al., 2015), being this species widely distributed not only in remote, but also in urban and industrial sites (Maisto et al., 2013). In relation to its characteristics of Mediterranean evergreen sclerophyllous species, Q. ilex leaves are characterized by the presence of abundant hair (stellate trichomes) on the surface, able to capture particulate matter; for this reason, they are effectively used as biomonitors of persistent pollutants, particularly PTEs (Blanusa et al., 2015). With the aim to derive PTE concentration gradients across areas differing in anthropogenic pressure, the present research investigated the concentrations of 18 PTEs, grouped according to Farago (1994) and Rout et al. (2001) in macronutrients (Ca, K, Mg, P, S), micronutrients (Co, Cr, Cu, Fe, Mn, Na, Ni, V, Zn) and non-essential elements (Al, As, Cd, Pb), in Q. ilex leaves. Information obtained from biomonitoring allowed also deriving temporal PTE concentration gradients and estimating plant nutritional status. In particular, the temporal gradients were derived by comparing the acquired results with previous data obtained in 2002 (unpublished data) for several of the sites currently investigated. The nutritional status was estimated from nutrient concentrations in Q. ilex leaves and was related to anthropogenic pressure. To these ends, one-year old leaves of Q. ilex, a plant widely distributed in the Salerno municipality (Campania Region, southwestern Italy), were collected from 26 sites subjected to different anthropogenic

2. Materials and methods 2.1. Study area Salerno municipality (40°41′ N; 14°46′ E) has a surface of 59.85 km2 and an average elevation of 4 m a.s.l. A population density of 2238 inhabitants/km2 characterizes it (https://ugeo.urbistat.com/ AdminStat/en/it/demografia/dati-sintesi/salerno/65116/4). The town is located on the Gulf of Salerno, on the Tyrrhenian Sea, and it is characterized by a Mediterranean climate, with hot (30 °C in August) and dry summers, and mild (8 °C in January) and rainy winters; the total rain amount is nearly 1000 mm/year. The main wind directions in the studied area are reported in Baldantoni et al. (2014). Being Salerno an important junction for terrestrial and marine transports (its port is one of the most active of the Tyrrhenian Sea), its economy is mainly based on services industries (Minolfi et al., 2018). 2.2. Sampling and laboratory analyses According to the distribution of Q. ilex plants in the Salerno district, a total of 26 sites (2 in remote, 4 in residential, 17 in urban and 3 in industrial areas) was selected (Fig. 1). Sites, regardless to their typologies, were distributed upon 6 soil system types (Fig. S1), with a common presence of pyroclastic deposits (Minolfi et al., 2018). 2

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At each site, leaf sampling was performed in the last week of March 2016 on 4–8 Q. ilex trees, according to their availability, 25–40 cm DBH (diameter at breast height). All the 1-year old leaves from 4 small branches (approximately 4 cm diameter) per tree (cut by extendable telescopic pruning shears), directed towards each cardinal point in the 4 directions and located 4 m above the ground and on the outer part of the canopies (Markert, 1993), were manually collected and pooled together, in order to obtain a homogeneous sample. All samplings were carried out minimizing the contact with the leaf surface. Leaves from each site were characterized for their water content (Text S1). On the un-washed, manually pulverized (in china mortars, using liquid nitrogen) and oven-dried (75 °C to constant weight) leaves, PTE concentrations were determined, in triplicate. To this end, an acid mixture in a microwave oven (Milestone Ethos, Shelton, CT, USA) was employed to digest each subsample. In particular, 2 mL 50% HF (SigmaAldrich, Milano, Italy) and 4 mL 65% HNO3 (Sigma-Aldrich, Milano, Italy) were added to 250 mg of leaf material, and samples were mineralized employing a 6-step mineralization program: 250 W for 2′, 0 W for 2′, 250 W for 5′, 400 W for 5′, 0 W for 2′, 500 W for 5′. After digestion, the solutions were diluted to a final volume of 50 mL, using milli-Q water (Millipore Elix 10, Darmstat, Germany). Macronutrient (Ca, K, Mg, P, S), micronutrient (Co, Cr, Cu, Fe, Mn, Na, Ni, V, Zn) and non-essential element (Al, As, Cd, Pb) concentrations were quantified by inductively coupled plasma optical emission spectrometry (PerkinElmer Optima 7000DV, Wellesley, MA, USA). Standard reference material (1575a pine needles) from NIST (2004) was analyzed to check the method accuracy. If the concentration of each element in the standard reference material was beyond the certified range, the recovery percentage in the standard reference material (ranging from 83 to 105 %) was used to correct the quantification of the investigated PTE in the samples. The method precision, calculated as relative standard deviation based on sequential measurements (n = 9) of the same sample for each element, ranged from 2 to 7 %, depending on the element.

Fig. 2. NMDS biplot with the superimposition of confidence ellipses (for α = 0.05) showing the differentiation among the four site typologies (green: remote areas, yellow: residential areas, red: urban areas, purple: industrial areas) as a function of the leaf PTE concentrations in each replicate of each sampling site within the Salerno municipality. For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.

overlap with their distribution within soil system types (Fig. S1), a contribution of the latter to the differentiation of site typologies can be excluded. Instead, soil characteristics might have only increased the variance within each site typology but, due to the generalized occurrence of carbonates and pyroclastic deposits (Minolfi et al., 2018), even this contribution can be estimated to be of little relevance to the observed pollution patterns. Among the macronutrients analyzed (Fig. 3), only K showed significant (P < 0.010) differences among site typologies (Table 1), with the highest mean concentrations observed in remote areas. These differences are attributable to the highest K concentrations measured in one of the two remote sites (Fig. 3), the site 2 (on Mt. Bonadies, 300 m a.s.l.), the only one characterized by values higher than those of the chemical fingerprint of Q. ilex leaves (Bargagli et al., 1998). The high K concentrations in leaves from the site 2 may be due to a high percentage of readily exchangeable or available K. This occurrence may be related both to the soil K enrichment by throughfall and stemflow (Parker, 1983) and to local soil properties (Maisto et al., 2013). Also the other macronutrient (Ca, Mg, P, S) concentrations (Fig. 3) were in the same order of magnitude than the fingerprint values for Q. ilex leaves (Bargagli et al., 1998), indicating a good nutritional status in all site typologies. Anyway, only in few cases, macronutrients were related among them: S was positively (P < 0.010) correlated with P and negatively (P < 0.050) correlated with Ca (Table 2). All the micronutrients analyzed (Fig. 4), with the exception of Na and V, showed significant (P < 0.010 for Cr, Cu, Fe, Mn and Zn; P < 0.001 for Co and Ni) differences among site typologies (Table 1), with mean concentrations increasing in relation to the severity of anthropogenic pressure (remote < residential < urban < industrial areas). Notwithstanding industrial areas were characterized by the grater variability of these PTEs among sites (Fig. 4), according to the processing activity of each industrial plant, they were the unique for which significant (for α = 0.050) differences were generally (Co, Cr, Cu, Mn, Ni and Zn) highlighted, when compared to the other site typologies (Table 1). Moreover, all these micronutrients, with the exception of Zn (characterized by comparable values in leaves from all the

2.3. Data analysis The differentiation among the four site typologies (remote, residential, urban and industrial areas) as a function of the PTE concentration pattern in Q. ilex leaves, among the sampling sites, was evaluated by a non-metric multidimensional scaling (NMDS) based on two axes and the Manhattan distance metric, with the superimposition of the confidence ellipses (for α = 0.050). The differences in the concentration of each PTE among site typologies were evaluated through linear mixed models figuring the site typology as fixed factor and the site as random factor, using the Kenward-Roger test. Pairwise comparisons among site typologies were then performed by Tukey multiplicity adjustment (for α = 0.050). Finally, pairwise correlations between PTEs in Q. ilex leaves were tested according to the method of Spearman, due to the non-normal distribution of several variables, assessed through the Shapiro-Wilk test. All of the analyses were performed within the R 3.4.4 programming environment (R Core Team, 2018), using the functions of the “stats”, “lme4″ (Bates et al., 2015), “emmeans” (Lenth, 2018) and “vegan” (Oksanen et al., 2018) packages. 3. Results and discussion The NMDS biplot (Fig. 2) showed a clear separation of the confidence ellipses related to the four site typologies as a function of leaf PTE concentrations in each sampling site along the Salerno municipality. Whereas remote areas were characterized by relatively high concentrations of Cd, industrial areas were mostly characterized by relatively high concentrations of As, Mn, Ni and Pb. Urban, and to a lesser extent residential areas, were characterized by relatively high concentrations of all the other PTEs (Al, Ca, Co, Cr, Cu, Fe, K, Mg, Na, P, S, V and Zn). Since the distribution of sites within site typologies did not 3

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Fig. 3. Mean concentrations of Ca, K, Mg, P and S in Q. ilex leaves sampled from remote (green), residential (yellow), urban (red) and industrial (purple) sites along the Salerno municipality. The error bars represent the standard deviations of the means. In the upper and left corner of each graph, the box plots for each analyzed macronutrient in each site typology are also reported, with indication of the interquartile range (colored box), the upper and lower whisker (error bars), the outliers (circles), the mean (dotted horizontal line) and the median (solid horizontal line) values. Reference values for macronutrient concentrations in Q. ilex leaves (Bargagli et al., 1998) are: Ca =12 mg/g d.w., K =11 mg/g d.w., Mg =1.4 mg/g d.w., P =1.2 mg/g d.w., S =2.3 mg/g d.w. For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.

Table 1 Coefficients (F) of Kenward-Roger test, with the associated P-values (*: P ≤ 0.050, **: P ≤ 0.010, ***: P ≤ 0.001), performed on the concentrations of the 18 PTEs analyzed in Q. ilex leaves collected from remote, residential, urban and industrial sites. Mean concentrations (μg/g d.w.) of each PTE in each site typology and results from the pairwise comparisons of the estimated marginal means (using the Tukey multiplicity adjustment) are also reported: different letters indicate significant differences (for α = 0.050) among site typologies. PTE

F

remote

residential

urban

industrial

Al As Ca Cd Co Cr Cu Fe K Mg Mn Na Ni P Pb S V Zn

2.0266 2.2224 0.5952 3.4393 * 8.3403 *** 5.7796 ** 4.8232 ** 6.4210 ** 3.0597 ** 1.0593 7.258 ** 0.8684 7.8069 *** 1.2244 4.2512 * 0.6594 0.3334 6.3498 **

207.5 a ND 5005 a 0.21 a 0.05 b 0.30 b 3.60 b 134.4 b 9442 a 2025 a 40.91 b 188.29 a ND 949 a 0.09 b 1800 a 9.51 a 18.5 b

297.0 a 0.001 a 4475 a 0.07 ab 0.07 b 0.58 b 3.80 b 188.9 b 7079 ab 2191 a 27.13 b 209.78 a ND 1233 a 0.09 b 2152 a 10.55 a 18.0 b

374.6 a 0.012 a 3908 a 0.07 b 0.10 b 1.11 b 7.89 b 341.7 ab 6568 b 2220 a 65.50 b 382.43 a 0.16 b 1161 a 0.29 b 2186 a 10.93 a 22.4 b

425.0 a 0.052 a 4091 a 0.09 ab 0.21 a 2.32 a 19.01 a 547.5 a 6661 ab 1449 a 283.19 a 366.56 a 1.14 a 1192 a 1.73 a 2230 a 9.29 a 35.6 a

ND: not detectable.

in close proximity of a cast iron foundry (Fonderie Pisano & C. S.p.A.), were characterized by 1.5-fold higher Cr concentrations and by 4-fold higher Fe concentrations (Bargagli et al., 1998). Generally, the Fegroup elements are the primary PTEs associated with iron foundry dust, originating mainly during fettling and shake-out (Zhang et al., 1985). Among the industrial sites, leaves collected from the site 25 (Figs. 1 and 4), along the main road access of a cement plant (Italcementi Group), were characterized by 4.5-fold higher Mn concentrations than the fingerprint value (Bargagli et al., 1998). Highest Mn concentration were already measured in this site in a previous biomonitoring study aimed at evaluating air quality near the Italcementi Group plant, using Q. ilex leaves (Baldantoni et al., 2014); anyway, the concentrations previously measured (218 ± 4 μg/g d.w.) were 3-fold lower (Fig. 4). Considering that Mn is among the major PTEs emitted from cement plants (Gupta et al., 2012), it is possible to hypothesize either a greater activity by the Italcementi Group plant or the reduction in PTE removal efficiency, or even the use of different raw materials in the last years. Leaves collected from the site 26 (Figs. 1 and 4), near the clinker processing and storage (Baldantoni et al., 2014) of the Italcementi Group plant, were characterized by 2-fold higher Cr and Ni concentrations, and by 3-fold higher Cu concentrations than the fingerprint values (Bargagli et al., 1998). The highest Cr and Ni concentrations measured in this site were already observed in the previous air biomonitoring study in the area near the Italcementi Group plant (Baldantoni et al., 2014); anyway, a reduction in Cr (6.6 ± 0.2 μg/g d.w.) and Ni (6.8 ± 2.6 μg/g d.w.) concentrations has been recently observed (Fig. 4). Considering that Cr

sites), showed concentrations higher than those of the chemical fingerprint (Bargagli et al., 1998) only in leaves from industrial areas (Fig. 4). In particular, leaves collected from the site 24 (Figs. 1 and 4), 4

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Table 2 Spearman coefficients and P values (*: P < 0.050, **: P < 0.010, ***: P < 0.001) of pairwise correlations between the 18 PTEs analyzed in Q. ilex leaves.

As Ca Cd Co Cr Cu Fe K Mg Mn Na Ni P Pb S V Zn

Al

As

Ca

Cd

Co

Cr

Cu

Fe

K

Mg

Mn

Na

Ni

P

Pb

S

V

0.42* −0.07 −0.11 0.80*** 0.60** 0.49* 0.79*** 0.06 0.06 0.01 0.37 0.08 −0.08 0.47* 0.10 0.27 0.52**

−0.17 −0.20 0.43* 0.31 0.43* 0.40* 0.05 −0.32 0.31 0.28 0.08 0.15 0.15 0.24 −0.16 0.32

0.57** −0.10 −0.41* −0.50** −0.19 −0.02 0.03 −0.09 −0.47* −0.35 −0.07 −0.37 −0.45* −0.02 −0.11

−0.12 −0.17 −0.29 −0.07 0.01 0.34 −0.18 −0.19 −0.18 −0.34 0.02 −0.39* 0.35 −0.08

0.74*** 0.76*** 0.90*** −0.09 −0.15 0.30 0.45* 0.49* 0.16 0.56** 0.23 0.10 0.61**

0.87*** 0.89*** −0.05 −0.02 0.31 0.56** 0.60** 0.27 0.85*** 0.35 0.26 0.62***

0.83*** −0.15 −0.06 0.42* 0.67*** 0.62*** 0.35 0.73*** 0.49* 0.18 0.65***

−0.08 0.06 0.32 0.48* 0.45* 0.15 0.76*** 0.27 0.33 0.70***

−0.13 −0.17 −0.09 −0.10 −0.03 0.01 −0.10 −0.11 −0.10

−0.45* 0.04 −0.37 −0.20 0.17 −0.19 0.92*** −0.16

0.09 0.45* 0.27 0.13 0.14 −0.37 0.35

0.25 0.36 0.44* 0.35 0.17 0.47*

0.13 0.57** 0.25 −0.13 0.43*

0.04 0.50** −0.17 0.31

0.20 0.44* 0.59**

−0.01 0.43*

0.10

typologies, Cd showed the highest (for α = 0.050) mean concentrations in remote areas. Consequently, Al was positively correlated (P < 0.050) with both As and Pb (Table 2). The different behavior between Cd and Pb reflects the findings of a comprehensive biomonitoring study (De Nicola et al., 2017b) aimed at evaluating long temporal trends (approximately 20 years) in PTEs concentrations in Campania Region, by means of Q. ilex leaves. Since these two non-essential elements are linked to different air particulate sizes (fine for Cd and coarse for Pb), Cd leaf concentrations reflect the transport of fine particulate from urban or industrial areas, and Pb leaf concentrations mainly reflect local emissions (De Nicola et al., 2017b). Anyway, whereas Cd concentrations were everywhere comparable to the fingerprint value for Q. ilex leaves (Bargagli et al., 1998), Pb concentrations exceeded the fingerprint value at the site 24, in close proximity of the cast iron foundry, with concentrations 4-fold higher (Fig. 5). These results demonstrate that the airborne dusts from this industrial plant are an important source of Pb, as previously highlighted by a passive biomonitoring study of the main urban river crossing the Salerno town (Baldantoni and Alfani, 2016). Finally, Al concentrations (Fig. 5) were everywhere one order of magnitude higher than the fingerprint value (Bargagli et al., 1998), highlighting that Al, a main component of several common pedogenic minerals in Campania Region, is even in bioavailable forms (Buccianti et al., 2015), probably in relation to soil acidity (Maisto et al., 2004). Overall, remote, residential and urban sites of the Salerno municipality showed Cd, Cr, Fe and Pb leaf concentrations (Figs. 4 and 5) in the same order of magnitude than those measured in Q. ilex leaves from other 43 sites of Campania Region, grouped in the same site typologies, analyzed on a time period of 20 years (De Nicola et al., 2017b). Moreover, whereas Cd showed constant concentrations along time in all the site typologies, Cr, Fe and Pb showed a decrease in urban sites, as previously highlighted in Campania region since 2009 for Cr and Fe, and since 2002 for Pb (De Nicola et al., 2017b). This observation is further supported by comparing PTE concentrations obtained in this study with those previously measured (unpublished data) using the same methods in 1-year old Q. ilex leaves sampled in March 2002 in the same sites of the Salerno municipality (Table S1). In particular, a remarkable decrease (up to 2 orders of magnitude) in Cu, Ni, Pb and Zn concentrations was observed in all the site typologies (Figs. 4 and 5; Table S1). This finding reflects the general decline in PTE air concentrations observed in the Mediterranean area, and in Europe in general (EEA, 2018), as an effect of the implementation of abatement strategies of air pollutants in recent decades and the general decline in their emissions (Harmens et al., 2015), due for example to the use of unleaded fuels (De Nicola et al., 2017b). It is interesting to point out that neither micronutrients (Fig. 4) nor non-essential elements (Fig. 5)

and Ni are poorly volatile, these PTEs are totally incorporated into clinker (Ciobanu et al., 2017), so powder deposits on leaf surfaces greatly contribute to Cr and Ni leaf concentrations. In this context, the reduction in Cr and Ni concentrations observed along time, leaves standing up the only hypothesis of different raw materials employed by the Italcementi Group plant in the last years. Apart from the highest concentrations of most micronutrients (Co, Cr, Cu, Fe, Mn, Ni, Zn) in industrial areas, the general trend observed in mean concentrations among site typologies reflects the severity of anthropogenic pressure, as previously highlighted employing Q. ilex leaves to monitor PTE concentrations in different areas of Campania Region (Alfani et al., 2000; De Nicola et al., 2017b). By contrast, the high concentrations of Na and V measured in leaves collected from all the site typologies (Fig. 4), up to one order of magnitude higher than those of the chemical fingerprint (Bargagli et al., 1998), may have concealed differences attributable to the anthropogenic pressure. Taking into account that the Salerno municipality is located in front of the sea (Fig. 1), high leaf Na concentrations were expected (Maisto et al., 2013), in relation to the influence of sea salt depositions (Bussotti et al., 2000). The effects of sea spray are clearly highlighted by the lowest Na concentrations measured in the urban sites (7, 11, 12, 23) far away from the sea (Figs. 1 and 4). In this context, compared to the other industrial sites, the relatively high Na concentrations measured in the site 24 (Fig. 4), far away from the sea (Fig. 1), may be attributable to the influence of the cast iron foundry. Indeed, it is known that Na, together with other La-group elements, is primarily generated by pouring, shake-out and molding process, and it is thus associated with large particles emitted by iron foundries (Zhang et al., 1985). The high V concentrations observed in leaves collected from all the site typologies may be related to the volcanic nature of the soils in the investigated area (Minolfi et al., 2018). Moreover, as recently demonstrated (Orecchio et al., 2016), apart from the high total concentration of this element in soil, volcanic areas are characterized by high V percentages in exchangeable fractions or, in general, in bioavailable fractions. Whereas V was not correlated (for α = 0.050) with any of the other micronutrients analyzed and Mn was positively correlated (P < 0.050) with only Cu and Ni, all the other micronutrients (with the exception of Ni and Na) were positively correlated (P < 0.050 for Co-Na, Co-Ni, Fe-Na, Fe-Ni, Zn-Na, Zn-Ni; P < 0.010 for Co-Zn, Cr-Na, Cr, Ni; P < 0.001 for all the others) to each other (Table 2), indicating common sources of these elements. Among the non-essential elements analyzed (Fig. 5), only Cd and Pb showed significant (P < 0.050) differences among site typologies (Table 1). Whereas Pb (but also Al and As) showed mean concentrations increasing in relation to the severity of anthropogenic pressure (remote < residential < urban < industrial areas), with significant (for α = 0.050) differences between industrial areas and the other site 5

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Fig. 4. Mean concentrations of Co, Cr, Cu, Fe, Mn, Na, Ni, V and Zn in Q. ilex leaves sampled from remote (green), residential (yellow), urban (red) and industrial (purple) sites along the Salerno municipality. The error bars represent the standard deviations of the means. In the upper and left corner of each graph, the box plots for each analyzed micronutrient in each site typology are also reported, with indication of the interquartile range (colored box), the upper and lower whisker (error bars), the outliers (circles), the mean (dotted horizontal line) and the median (solid horizontal line) values. The asterisks indicate undetectable values. Reference values for micronutrient concentrations in Q. ilex leaves (Bargagli et al., 1998) are: Co = 0.23 μg/g d.w., Cr = 1.80 μg/ g d.w., Cu = 13.5 μg/g d.w., Fe = 200 μg/g d.w., Mn = 124 μg/g d.w., Na = 160 μg/g d.w., Ni = 1.0 μg/g d.w., V = 0.68 μg/g d.w., Zn = 54.5 μg/g d.w. For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.

highlights that diffuse, rather than local, contamination sources, such as vehicular traffic, mainly contribute to PTE concentrations observed in the studied urban area. This finding may be further supported by comparing mean micronutrient and non-essential element

showed remarkably high concentrations in leaves from specific urban sites of the Salerno municipality (Fig. 1), such as the site 7 (in an area previously affected by fire), the site 10 (in close proximity of a petrol station), or the site 23 (along the motorway). This observation 6

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Fig. 5. Mean concentrations of Al, As, Cd and Pb in Q. ilex leaves sampled from remote (green), residential (yellow), urban (red) and industrial (purple) sites along the Salerno municipality. The error bars represent the standard deviations of the means. In the upper and left corner of each graph, the box plots for each analyzed non-essential element in each site typology are also reported, with indication of the interquartile range (colored box), the upper and lower whisker (error bars), the outliers (circles), the mean (dotted horizontal line) and the median (solid horizontal line) values. The asterisks indicate undetectable values. Reference values for non-essential element concentrations in Q. ilex leaves (Bargagli et al., 1998) are: Al = 47.6 μg/g d.w., Cd = 0.4 μg/g d.w., Pb = 1.04 μg/g d.w. For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.

(Fig. 4), and Al (Fig. 5), all PTEs associated with vehicular traffic emissions (Marié et al., 2010; Jandacka et al., 2017), showed the highest concentrations in the site facing the road. Anyway, as previously described, all PTE concentrations in urban area of the Salerno municipality fall in the natural background concentrations for Q. ilex leaves (Bargagli et al., 1998). It is important to emphasize that the capability of Q. ilex leaves, due to their morphological and physiological characteristics, to capture particulate-bond contaminants on the surface or to accumulate them in the interior tissues, can be potentially used in air filtering to remove pollutants, as previously reported for other oak species (De Nicola et al., 2017a). 4. Conclusions The concurrent analysis of several PTEs in Q. ilex leaves sampled in remote, residential, urban and industrial sites of the Salerno municipality, in the Mediterranean area, allowed obtaining accurate information on spatial and temporal air pollution gradients, as well as on the plant nutritional status. In particular, a good nutritional status in all the site typologies was observed, highlighting an adequate nutrient supply from soil, also in areas heavily affected by anthropogenic activities. Among the site typologies, industrial sites were generally characterized by the highest concentrations of several PTEs, even if high values of selected PTEs (As, Mn, Ni and Pb) were spatially localized and attributable to specific industrial activities. Conversely, urban (and to a lesser extent residential) sites were mainly affected by diffuse and generalized pollution sources, such as vehicular traffic, rather than by local contamination sources. Even if relatively high concentrations of most PTEs were observed in the urban sites, their comparison with PTE concentrations measured in 2002 in Q. ilex leaves collected from the same sites belonging to all the four site typologies demonstrated a general decline in air concentrations, as generally observed in Europe. Finally, remote sites showed the highest Cd concentrations, likely in relation to the transport of fine particulate from industrial and urban areas. Apart from the observed gradients, the majority of PTEs in leaves from the Salerno municipality, showed concentrations in the same order of magnitude than the natural background concentrations for Q. ilex leaves. Conversely, the exceedingly high concentrations of Na as well as of Al and V in all the site typologies were attributable to natural sources: the proximity to the sea and the lithological characteristics of the area, respectively. The capability of Q. ilex leaves to trap particulate-linked pollutants can help planners both to detect contamination gradients during environmental quality monitoring and to mitigate air contamination in critical areas. Compliance with ethical standards The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. All the authors read and approved the final version of the manuscript.

concentrations in leaves collected from the site 13, in the inner area of the main hospital in Salerno, with those relative to the site 14, in an area of the same hospital facing the road (Fig. 1). Co, Cr, Cu, Fe, Mn, Na 7

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