In the Panasqueira mine area, Arbutus unedo L. (arbutus tree) grows on soils developed on waste materials and on soils impacted by mining activity. The arbutus berry brandy is considered a product with economic value. The aims of this study were to evaluate the biogeochemical impact of the mining activity on soils and arbutus trees, to assess the possible risks associated with human consumption of the fruits and the derived brandy, and to evaluate the potential of the arbutus tree in phytostabilization.
Materials and methods
Soil samples (10–15 cm deep) developed on waste materials, on schists affected by seepage water or treatment plant effluents and on colluvium-alluvium materials were characterized (fraction <2 mm) for pH, particle size distribution, organic carbon (Corg), cation exchange capacity (CEC) and NPK by classical methodologies. Plant (A. unedo) samples (roots, leaves and twigs, and fruits) were collected at the same sites as the sampled soils, washed with tap and distilled water and dried at 40 °C. The elements’ concentrations in soils (total fraction—four-acid digestion and available fraction—diethylenetriaminepentaacetic acid extraction), plants (ashing followed by acid digestion) and brandy samples produced with fruits collected on contaminated and non-contaminated sites were determined by inductively coupled plasma atomic emission spectroscopy.
Results and discussion
The soils are mainly acid, silty loam, with variable values for Corg, CEC and NPK. They are contaminated with As (158–7,790 mg/kg), Cd (0.6–79 mg/kg), Cu (51–4,080 mg/kg), W (19–1,450 mg/kg) and Zn (142–12,300 mg/kg). The available fraction of the soils is quite variable between <0.04 and 76 % of the total, depending on the element. Trace elements’ concentrations, in leaves and twigs, are within the normal range for plants, except for Cd and Zn that, in some samples, are above the normal values, but without phytotoxic symptoms. Trace elements’ concentrations in fruits are low. The calculated hazard quotient for all trace elements in arbutus berry was <0.1. In the brandy, elemental concentrations are within the legal standards, except for Pb, whose higher concentrations may result from distillery equipment.
According to the EC 466/2001 legislation and with a hazard quotient of <1, the arbutus berry consumption does not constitute health risks for humans. The fruits can be used to produce local brandy. The concentration of copper in brandy is within the range established by the Portuguese legislation. Arbutus unedo can be used in the phytostabilization programs in the Panasqueira area, for it is a pioneer species and a non-accumulator of trace elements.
The world famous Panasqueira tungsten and tin mine is one of the few mines still operating in Portugal in the twenty-first century. This mine has been operating continuously since 1896, apart from a brief period at the end of the World War II and in the mid-1990s. The ore exploitation has generated large amounts of waste materials, which were disposed on the landscape constituting huge tailings, giving rise to a strong visual impact. Active waste heaps steadily increasing every day are bared. Older (30–80 years old) and relatively recent (5–10 years old) tailings, where soils have been developed, present vegetation cover, mainly composed of pine trees (Pinus pinaster Aiton), arbutus trees, also known as strawberry trees (Arbutus unedo L.) and several shrubs belonging to the genera Calluna, Cistus, Cytisus, Erica, etc. (Abreu and Magalhães 2009). The waste materials contain high concentrations of hazardous elements, namely As (466–12,000 mg/kg), Cd (2.6–87 mg/kg), Cu (214–3,741 mg/kg), W (40–12,000 mg/kg) and Zn (340–4,224 mg/kg) (Ávila et al. 2008; Godinho 2008).
Arbutus unedo that belongs to the Ericaceae family is a perennial plant, which usually presents small dimensions, but it can occasionally reach 9 m tall and 8 m wide (Noronha 2001), as is the case in the Panasqueira mine area. This Mediterranean shrub is known by its ornamental, meliferous and medical (laxative effects, antiseptic and diuretic properties, to treat cardiovascular pathologies, diabetes and inflammatory conditions) importance (Afkir et al. 2008; El Haouari et al. 2007; Mekhfi et al. 2006; Oliveira et al. 2011; Silva 2007). According to Malheiro et al. (2012), A. unedo leaves are a potential source for natural compounds, mainly polyphenolic compounds, which have significant bioactive properties that can be explored by the pharmaceutical, chemical and food industries. The mature arbutus berries are extremely sweet (high fructose content, Barros et al. 2010), being edible and frequently used to produce sweets, jam, jellies and brandy by their fermentation and distillation. It is common knowledge that eating a few arbutus berries causes signs of drunkenness, and owing to this fact, they are considered rich in ethanol. As noted by Molina et al. (2011), there is no reference, in the scientific literature, to the presence of ethanol in these fruits. Fruits are a very good source of health promoter compounds having a wide range of antioxidants, including vitamin C and E, niacin, carotenoids, polyphenolic compounds, dietary fibre and omega-3 polyunsaturated fatty acids (Alarcão-e-Silva et al. 2001; Barros et al. 2010; Oliveira et al. 2011; Pallauf et al. 2008; Ruiz-Rodríguez et al. 2011).
Despite all the referred possible uses of this plant species, the brandy is, nowadays, an economic value-added product (DGRF 2005). The brandy is a traditional beverage known in Portugal as Aguardente de medronho produced in small- or industrial-scale units, being an important social agro-sustainable business (Alarcão-e-Silva et al. 2001; Santo et al. 2012; Soufleros et al. 2005).
In the Panasqueira mine area, over and above the social and economic interest of the A. unedo, this shrub may also have a potential to be used in the phytostabilization of degraded soils and waste heaps due to the observed good vegetative development. Moreover, in order to be used in phytostabilization programs, this shrub cannot be an accumulator of hazardous elements in shoot tissues (leaves, twigs, fruits and seeds), once it can be consumed by humans and/or animals (Mendez and Maier 2008; Prasad and Freitas 2003).
Phytostabilization is a soil/waste remediation technology whose strategy is to create a vegetative cover for long-term stabilization and contaminant containment, aiming to reduce risks to human health and environment. The plant canopy reduces aeolian dispersion of particles, and roots prevent water erosion, immobilize hazardous elements and provide a rhizosphere environment where elements can be stabilized (Abreu and Magalhães 2009; Mendez and Maier 2008). This is achieved using specific tolerant and well-adapted plants, as it appears to be the case of arbutus tree.
Considering that the waste materials in the Panasqueira mine area have high concentrations of hazardous elements, attention should be paid to the possible risks to the human health arising from a potential soil-to-plant transfer of those chemical elements and their translocation from the roots to the shoots, with particular regard to the fruits. The aims of this study were to evaluate the biogeochemical impact of the mining activity on soils from the Panasqueira mine area, mainly those developed on waste materials, as well as on A. unedo growing on these soils; to access the possible risks for human health linked to the consumption of the leaves and twigs, arbutus berries and the derived brandy; and also to evaluate the potential of arbutus tree in the phytostabilization of the contaminated soils and tailings of Panasqueira.
Materials and methods
The Panasqueira mine is located in Central Portugal, Beira Interior region, at approximately 300 km north-east of Lisbon and 200 km south-east of Porto City. The Panasqueira tungsten and tin deposit is reported to be the largest quartz vein deposit in Europe related to hydrothermal mineralization associated with Hercynian plutonism (Cavey and Gunning 2006). This deposit is located in a folded metasedimentary sequence, the Beira-Schist Formation of the upper Precambrian-Cambrian age. The Panasqueira ore deposit consists of a series of stacked, subhorizontal, hydrothermal quartz veins intruding into the Beira-Schist Formation containing mainly wolframite, arsenopyrite, chalcopyrite and cassiterite (Corrêa de Sá et al. 1999). Intrusive is an important component to the mineralizing events at Panasqueira; a granite intrusion is thought to be the principal source of the mineralizing fluids responsible for the economic wolframite vein system (Thadeu 1951). The mineralized zone has a dimension of around 2,500 m in length, and the width varies from 400 to 2,200 m and reaches to at least 500 m in depth (Cavey and Gunning 2006; Corrêa de Sá et al. 1999). Wolframite mineralization occurs as large aggregates of crystals or very large crystals usually concentrated towards the margins of the quartz veins or, occasionally, close to the central portion of the quartz veins (Corrêa de Sá et al. 1999).
The Panasqueira mine area includes three subareas: Cabeço do Peão and Panasqueira, which are nowadays inactivated, and Barroca Grande where the present and active underground mine processing plant is located. The Barroca Grande site includes underground mine and portals, the active processing plant, mine offices and employees’ housing, in addition to the active tailings’ disposal areas, two mud dams and the Salgueira water treatment plant (Cavey and Gunning 2006).
The active heaps extend along more than 1 km south-east from the mine portals in the north river side of the Bodelhão stream that drains the Barroca Grande subarea to the Zêzere River. These heaps present steep slopes; they are bared and composed of gravel, stones and sand materials containing high concentrations of hazardous chemical elements associated with arsenopyrite and other ore minerals (Ávila et al. 2008). On the surface of the inactive tailings (30–80 years old or even younger (>5 years old)), a thin layer of soil (Spolic Technosol Toxic, IUSS Working Group WRB 2007) was developed supporting a vegetation cover. Part of the vegetation was planted to feed the paper industry (pine trees), but spontaneous plants, like arbutus tree, heathers, rockrose and brooms, also colonized those tailings.
Soil sampling and analysis
Thirteen (10–15 cm deep) samples of soils, developed over tailings, over schist that receives the influence of seepage water or treatment plant effluents, and on colluvium-alluvium materials, were collected on April and November 2007 and March 2008 in the surrounding area of Barroca Grande (Fig. 1). These soils, classified as Spolic Technosol Toxic (IUSS Working Group WRB 2007), were considered as representative of the different soils where arbutus trees grow.
Soil samples (fraction <2 mm) were characterised as follows: pH in water suspension (1:2.5 m/v), particle size distribution by sieving and sedimentation, organic carbon (Corg) by dry combustion (Ströhlein method), cation exchange capacity (CEC) and exchangeable cations by 1 mol/L ammonium acetate at pH 7 (Póvoas and Barral 1992), extractable phosphorous and potassium (Égner et al. 1960), mineral nitrogen (Keeney and Nelson 1982), iron from iron oxides (De Endredy 1963) and manganese from manganese oxides (Chao 1972). The same fraction of each soil sample was analysed for elemental total concentrations by inductively coupled plasma atomic emission spectroscopy (ICP) and instrumental neutron activation analysis (INAA) after four-acid digestion (perchloric acid + nitric acid + hydrochloric acid + hydrofluoric acid), in a certified laboratory (Activation Laboratories 2010a, ISO/IEC 17025). Soil available fraction of the same chemical elements was determined by ICP after extraction with diethylenetriaminepentaacetic acid (DTPA) aqueous solution (0.005 mol/L DTPA + 0.1 mol/L triethanolamine (TEA) + 0.01 mol/L calcium chloride; Lindsay and Norvell 1978).
Plant sampling and analysis
Representative samples of arbutus trees’ aerial parts (leaves and twigs—13 samples) and roots (six samples) as well as six samples of fruits (arbutus berries) were collected from plants growing on the above-described soil sampling places (Fig. 1). Leaves and twigs, and roots were washed in abundant tap water and rinsed with deionised water, dried at 40 °C, homogenised and finely ground. Before drying, roots were also cut in small pieces and rewashed with deionised water in an ultrasound-assisted bath for 30 min. In order to copy the fruits’ fermentation conditions traditionally used by local farmers, the arbutus berries were not washed before being dried.
In the plant samples, the total concentrations of the same chemical elements that were analysed in soils were determined by ICP/MS, after ashing (480 ºC) and acid digestion (HNO3 and H2O2) (Activation Laboratories 2010b).
Three brandy samples distilled from arbutus berries collected by local brandy producers, from plants growing on contaminated soils (BAL 1) and on soils of the surrounding area (Panasqueira) but with no contaminant influence (BAL 2 and BAL 3), were analysed by ICP. The brandy was produced in small local private distilleries for personal consumption.
Statistical analysis (regression equations) was performed using the Excel for Windows (Microsoft Office Excel 2003) in order to correlate chemical elements’ concentrations in soils and plants. The quality control of the multielementar chemical analysis was done by the Activation Laboratories (international certified laboratory, ISO/IEC 17025).
Soil-to-plant transfer coefficient (TransferC) characterizes the uptake capacity and accumulation of a specific chemical element in the aerial part of the plant. This coefficient was calculated as follows: TransferC = [total leaves and twigs element] / [total soil element]. The plant capacity to absorb a chemical element from the soil, when it occurs in an available form (water soluble or water soluble plus exchangeable) for plants determined after soil chemical extraction using an appropriated solution, can be expressed as the bioconcentration coefficient (BC). This coefficient represents the level of plant tolerance for a potential toxic element, the plant being considered tolerant when BC > 1 (Abreu et al. 2008), and it was calculated as follows: BC = [leaves and twigs element] / [element available soil fraction, extracted with DTPA aqueous solution]. The translocation coefficient (TranslC = [total leaves and twigs element] / [total roots element]) evaluates the plant capacity to translocate a chemical element from roots to aerial parts. According to Bu-Olayan and Thomas (2009) and McGrath and Zhao (2003), plants are considered accumulators of a trace element if the calculated soil–plant transfer coefficient is higher than one.
Health risk assessment methods can be based on the hazard quotient (HQ), a ratio between the estimated exposure dose of a specific contaminant and its oral reference dose (RfD), defined by U.S. EPA as the maximum acceptable oral dose of a toxic substance (U.S. EPA 2000). The HQ assumes that there is a level of exposure below which it is unlikely, even for sensitive populations, to experience adverse health effects during lifetime. If the HQ exceeds unity, there may be a concern for potential non-carcinogenic health effects. But if HQ does not exceed unity, it is assumed that no chronic risks are likely to occur. To calculate the HQ, it is necessary to estimate the element exposure dose from fruits or leaves and twigs ingestion pathway (EDing). For each chemical element, the exposure dose (milligrams per (kilogram-day)) and the HQ value was defined as follows (U.S. EPA 1989, 2000):
where C is the mean element concentration in fruit or leaves and twigs samples (milligrams per kilogram), F i is the food ingestion rate per person (kilograms per day), E d is the exposure duration (in this study, equivalent to the average adult lifetime, years), E f is the exposure frequency (days per year), W is the average body weight (kilograms), T e is the average exposure time for non-cancer risk (E d × 365 days) and RfD is the oral reference dose (milligrams per kilogram per day).
The potential non-cancer risk of the populations for exposure to As, Cd, Cu and Zn, on using arbutus leaves and twigs for the preparation of infusions or consuming the arbutus berries from the Panasqueira mine area, was evaluated. The HQ for W and Pb was not calculated once there is no known oral reference dose for these chemical elements (ASTSWMO 2011; U.S. EPA - IRIS 2004).
Results and discussion
Soil characteristics (pH, particle size distribution, organic carbon, iron and manganese in their oxides, cation exchange capacity, extractable phosphorous and potassium and mineral nitrogen) are presented in Table 1.
Panasqueira mine soils are mainly acidic (3.83 ≤ pH ≤ 5.90), except soil PAN 9S with pH = 8.30, which was developed on waste materials covered by a yellow-orange mud, from the rupture of the pipe conducting effluent from the mine water treatment plant (where water was treated with lime) to a pond. From the values of the particle size distribution, the soils’ texture can be classified mainly as silty loam. The concentration of organic matter (OM = Corg × 1.724) in the soils is considered high (41 ≤ OM ≤ 60 g/kg) or very high (OM ≥ 61 g/kg) (INIA - LQARS 2000). The soils present cation exchange capacity values ranging from 12.9 to 48.5 cmolc kg−1 that are probably a consequence of their organic matter richness. In spite of the low concentrations of Ca (0.11–6.96 cmolc kg−1) and Mg (0.07–3.47 cmolc kg−1) in the exchangeable complex, these are the dominant exchangeable cations in the studied soils. The soil PAN 9S has very high values for the concentrations of exchangeable Ca (30.32 cmolc kg−1) and Mg (27.67 cmolc kg−1) as a result of the composition of the mud from the water treatment plant.
Panasqueira mine soils are rich in extractable K, with the sample PAN 15S showing the lowest value (Table 1), which according to INIA - LQARS (2000) is classified as a soil having medium fertility (41–85 mg K kg−1). The soils have variable concentrations of extractable P and mineral N (11.5 ± 6.3 mg N kg−1). Regarding the extractable P, soils PAN 10S and PAN 15S have the highest fertility rate (>90 mg P kg−1), the soils PAN 4S and PAN 9S have medium and high fertility, respectively (21–45 and 46–90 mg P kg−1), whereas the remaining soil samples can be classified as having low (<20 mg P kg−1) and very low (≤10 mg P kg−1) fertility (INIA - LQARS 2000).
The soils contain relatively high amounts of iron oxides (Table 1), reflecting the mineralogy and chemical composition of the wastes. Contrasting with iron oxides, the manganese oxides are less abundant.
All soil samples are considered to be contaminated with As (Table 2) once its total concentration exceeds largely the maximum allowed value (MAV) for soils and for agriculture use (12 mg As kg−1, CCME 2007). Ávila et al. (2008) identified arsenopyrite as the main sulfide mineral that has been rejected after ore processing, being part of the waste materials. Arsenopyrite (FeAsS), similarly to what occurs with other minerals containing Fe(II), is unstable when subjected to oxidizing environments in the weathering crust, giving rise to iron oxides and the release of several chemical elements, which can be spread to the surrounding environments.
The soils can also be considered contaminated with Cd, Cu, Pb and Zn, as more than 50 % of the soils (Table 2) have total concentrations of those elements above the MAV according to the Canadian legislation (CCME 2007; 1.4 mg Cd kg−1, 63 mg Cu kg−1, 70 mg P kg−1 and 200 mg Zn kg−1). Cadmium is found in most zinc ores (Greenwood and Earnshaw 1995), and for the analysed soils, a strong positive correlation was found between the total concentrations of Zn and Cd (R 2 = 0.8495, Table 3). The values found suggest that, in the Panasqueira mine, Zn and Cd should be found in the same ore, similarly to the most occurrences.
The soil sample PAN 9S, owing to its elemental composition (Table 2), can be considered not a representative of the soils in the area because of the particular influence of the lime-treated sewage from the leaking pipe on the tailing materials where the soil was developed, as was explained before. This soil presents high total concentrations of Cd, Cu and Zn (Table 2), and the available fraction (DTPA extracted) attained 53 % for Cd and Zn and 39 % for Cu, of their total concentrations. Although the total concentrations of Cd, Cu and Zn in the soil sample PAN 10S are lower than those in the sample PAN 9S, the soil PAN 10S has higher Cd and Zn soil available fractions (76 and 60 % of the total, respectively), but Cu has similar values (~38 % of the total) in both soils. In spite of the geographical proximity of the above-referred soils, PAN 10S is only over the influence of direct drainage from the waste dump (Fig. 1). In opposition, the soil PAN 15S, which is developed on colluvium-alluvium materials, has much lower soil available fractions for the same chemical elements (Cd <4 %, Cu = 23 % and Zn = 4.5 % of the total) despite the similar total concentrations of those elements.
The majority of the soil samples had total concentrations of Pb which were within the allowed values for soils and agriculture use (70 mg Pb kg−1, CCME 2007). In spite of the higher concentrations of Pb in the soils PAN 6S and PAN 15S, the concentrations of this element in the soil available fraction are the lowest (Table 2). One possible explanation arises from the fact that these soils also have high concentrations of As and Fe, which can originate solid phases with very low solubilities as was also observed in soils from São Domingos mine (Santos et al. 2012). Although the Canadian legislation (CCME 2007) does not refer to the maximum allowed value for W, its total concentration in the majority of the soil samples (Table 2) exceeds the normal range in soils (0.5–83 mg W kg−1, Agency for Toxic Substances and Disease Registry 2005) and even the average concentration reported by Pyatt and Pyatt (2004) for soils in the vicinity of mining/smelting sites in North Queensland, Australia (56 and 78.4 mg W kg−1 for top and deeper soil, respectively). The soil available fraction of W is, for the majority of the samples, <1 % of the total concentration, which is probably a result of the low values of the soil pH. The exceptions are the soil samples PAN 1S, PAN 2S and PAN 9S, especially the latter one (pH = 8.3) where the available fraction attained 12 % of the total concentration of the element. This can be a consequence of the anion monomer species of W formation that occurs for pH > 6.2 (Koutsospyros et al. 2006).
The total concentration of Mn was, in general, in the normal range for soils (200–300 mg Mn kg−1, Srivastava and Gupta 1996), with a maximum value (8.9 g Mn kg−1) in the PAN 9S sample. The overall percentage of Mn in the available fraction is very small (<0.05 %), when compared with its total concentration.
The concentrations of the metals in the DTPA solutions used for the soil available fraction extraction are positively correlated to their total concentrations in the soil samples, laying the R 2 values in the range of 0.905–0.998 (Table 3). The correlation value for As was considerably lower (R 2 = 0.581).
Chemical elements’ concentrations in roots, shoots (leaves and twigs) and fruits of A. unedo are shown in Table 4. Concentrations of Al (143.8 ± 63.5 mg kg−1 dry matter) and Fe (<100 mg kg−1 dry matter for the majority of the samples) in leaves and twigs of arbutus trees are in the range considered normal for plants (50–200 mg Al kg−1 and 50–250 mg Fe kg−1, Srivastava and Gupta 1996) despite the high concentrations of these elements in the soil available fraction extracted with DTPA (Table 2). These elements are mostly accumulated in the roots of the plant as the calculated translocation factor from roots to shoots, for the majority of the plants, is lower than unity (Table 5).
The As concentrations in total and available fractions of the studied soils (Table 2) exceeded the toxic values for many plant species according to Srivastava and Gupta (1996; 25–100 and 2 mg As kg−1 for total and available fractions, respectively), but the concentrations in plant shoots (Table 3) are lower than the toxic range limit for the majority of plants (5–20 mg As kg−1, Kabata-Pendias 2011). Plants mainly accumulate As in roots (Tables 4 and 5). Arsenic concentrations in the studied arbutus trees’ shoots (leaves and twigs) are similar to those obtained by Moreno-Jiménez et al. (2008) for the same species growing under controlled conditions, while As concentration in roots is lower than that obtained by the above-referred authors.
Cadmium concentrations in leaves and twigs of 62 % of the collected plants (Table 4) are above the level considered tolerable for crops (0.05–0.2 mg Cd kg−1, Kabata-Pendias 2011). Plants growing on the soil PAN S9, which contains Cd above the critical toxic level (10–30 mg Cd kg−1 of soil, Srivastava and Gupta 1996), presented the highest Cd concentration (12.9 mg Cd kg−1 dry mass), which is already in the range of the excessive or toxic value for plants in general (Kabata-Pendias 2011). Concentration of Cd in the shoots is strongly correlated to the concentration of the element in soil (total and available fraction, R 2 = 0.878 and R 2 = 0.962, respectively; Table 3). Arbutus tree translocates Cd from roots to shoots (Table 5, median of the TranslC = 1.5), but this element was not translocated to the fruits (median of the TranslC shoots to fruits = 0.08).
Copper and Zn are essential trace elements for plants’ development, but if in excess, they cause toxicity disorders. Despite the high concentrations of Cu and Zn (ranging from 2.5 to 1,592 mg Cu kg−1 and from 3.6 to 6,471 mg Zn kg−1) in the soil available fraction of the soils from the Panasqueira mine area, A. unedo presented in the above-ground part of the plant low Cu concentrations, but above the lowest limit for deficiency (2 mg kg−1, Kabata Pendias 2011). Zinc concentrations in the shoots were, in general, within the range considered sufficient or normal for plants, but some samples showed concentrations within the excessive or toxic range (150–400 mg Zn kg−1, Kabata Pendias 2011) as is the case of the samples PAN 5, PAN 9, PAN 10 and PAN 15. In spite of the low concentrations of Cu or high concentrations of Zn in the plants, they did not present visual symptoms of disorders related to deficiency (Cu) or toxicity (Zn). This species translocates Zn to the aerial part whereas Cu has a variable behaviour depending on the sample (Table 5); plants growing on soils with high Cu concentration in the available fraction retain more Cu in the roots (PAN 9 and PAN 10, Tables 2 and 4).
Zinc and Cd ions are chemically similar, for both belong to the same group of the periodic table. Both are mostly found in the same ores being found together in the same environments (Greenwood and Earnshaw 1995). Srivastava and Gupta (1996) mentioned that in soils where the Zn/Cd ratio is high, the translocation of Cd to the plant shoots can occur, as a result of Zn effective competition for the sites of Cd fixation in the soils. Since in the analysed soils there is high Zn/Cd ratios and strong correlation between the total concentrations of Zn and Cd (Table 3), the same phenomenon could be expected to occur in the plants. In fact, for the plant shoots, a strong correlation was found between the total concentrations of Zn and Cd (R 2 = 0.884 considering all plant samples except PAN 9 that was an outlier, Table 3). It is well known that Cd2+ is able to substitute Zn2+ in many Zn0containing enzymes, this being one of the reasons why the ion Cd2+ is toxic (Lippard and Berg 1994). In spite of the high concentrations of Cd in the plants, they did not present visual symptoms of disorders related to the toxicity of Cd.
Lead concentrations (0.2–1.3 mg kg−1, Table 3) in the plant leaves and twigs samples are relatively low when compared to the values presented by Kabata-Pendias (2011) for various species (5–10 mg kg−1). The translocation of this element from roots to shoots in the studied species is low to very low (Table 5) as was also observed in other shrub species of the same Ericaceae family or the Cistaceae family (Abreu et al. 2008, 2012).
Manganese concentration in the above-ground part (leaves and twigs) of the plants was in the normal range found in the mature leaf tissues (30–300 mg kg−1, Kabata-Pendias 2011), except for the sample PAN 10 whose Mn concentration (673 mg kg−1) lies within the range considered excessive or toxic by Kabata-Pendias (2011). However, different species show different threshold levels for Mn toxicity (Srivastava and Gupta 1996). As other shrub species, A. unedo also translocates manganese from roots to shoots (Table 5, Abreu et al. 2012; Monaci et al. 2011).
The common range of W in terrestrial plants is, according to Kabata-Pendias (2011), lower than 0.15 mg kg−1, but some species growing on W-contaminated soils in the vicinity of abandoned mines can accumulate that element presenting highest concentrations of W, which can attain values of 13.6 mg kg−1 in Eucalyptus melanophloia (Pyatt and Pyatt 2004) and values of 30.7 mg kg−1 in Cistus ladanifer or 90.8 mg kg−1 in Digitalis purpurea (Pratas et al. 2005). The W concentrations (≤3.4 mg kg−1) in the shoots of the studied arbutus trees are lower than the values referred by Pratas et al. (2005) for other shrub species (Calluna vulgaris—9.74 mg W kg−1 and Erica umbellata—4.04 mg W kg−1) belonging to the same family (Ericaceae) of A. unedo. According to Koutsospyros et al. (2006), it appears that W accumulation by plants is directly related to its concentration in soils, but no significant correlation was found between W concentration in soils (total and available fraction) and A. unedo, although the plant sample (PAN 9) with the highest W concentration has been collected in the soil with the maximum concentration of the soil available fraction extracted with DTPA (71.2 mg kg−1, Table 2).
This species is not an accumulator of any of the analysed chemical elements as the calculated coefficient transfer soil to plant (TransferC) for each element is lower than unity (except three samples for Cd and one sample for manganese and Zn, Table 5). However, when this coefficient was calculated considering the concentration of the available fraction of the elements (BC), Mn and Zn showed values >1 (median values of 2.7 and 2.9, respectively; Table 5).
Arbutus unedo is a species with possible use in phytostabilization programs, as the majority of the hazardous chemical elements are mainly accumulated in roots. Although the concentration of Cd in shoots (leaves and twigs) is considered to exceed the normal range in plants, it does not exceed the toxic limit to cattle (10 mg Cd kg−1, National Research Council (NRC) 2005). Only the plant sample PAN 9 (12.9 mg Cd kg−1) exceeds this limit which is a result of the high concentration of the element in soil (total and available fractions). This species was already indicated by Moreno-Jiménez et al. (2008) as a useful species for the phytoremediation of semiarid degraded soils contaminated with As.
Arbutus unedo fruits
Chemical elements’ concentrations in arbutus berries are presented in Table 4. Comparing the elemental concentrations of the arbutus berries collected from plants growing on contaminated soils in the Panasqueira mine with the same elements concentrations in the fruits sampled in a non-contaminated area in Turkey (Özcan and Haciseferoğullari 2007), As, Pb and Cd had lower concentrations in the fruits from the mine area than from the non-contaminated area. However, Al, Zn and Cu had, in general, higher concentrations in the fruits from the contaminated mine area (15–124 and 20.11 ± 2.69 mg Al kg−1 for Panasqueira and Turkey, respectively; 7–14 and 8.09 ± 0.96 mg Zn kg−1 for Panasqueira and Turkey, respectively; and 2.4–3.2 and 1.65 ± 0.41 mg Cu kg−1 also for Panasqueira and Turkey, respectively). Also, arbutus berries collected in non-contaminated areas of Spain (Ruiz-Rodríguez et al. 2011) presented concentrations of Cu, Mn and Zn lower than those of the fruits collected both in Turkey and in the Panasqueira mine area.
The calculated shoots (leaves and twigs)-to-fruit translocation coefficient for the analysed chemical elements was low to very low (Table 5), except for Cu with TranslC close to or higher than unity (TranslC—mean value = 1.052).
The total concentration of Cd (<0.04 mg kg−1 fresh weight) in fruits is lower than the maximum allowed value (0.05 mg kg−1 fresh weight, Commission of the European Communities 2001) on vegetables and fruits. Total concentration of Pb in fruit samples (<0.05 mg kg−1 fresh weight) was smaller than the European Commission-defined maximum level for berries and small fruits including arbutus tree wild plants (0.2 mg Pb kg−1 fresh weight, Commission of the European Communities 2001). Therefore, according to the Commission of the European Communities (2001), the consumption of these fruits does not constitute a public health risk with regard to Pb and Cd concentrations as their concentrations are within the toxicologically acceptable ranges.
Arbutus berry brandy
Due to the absence of the European or Portuguese legislation that defines the maximum allowed levels of trace elements in arbutus berry brandy, apart from Cu (Decreto-Lei no. 238/2000), the concentrations of the determined chemical elements in the brandy were compared to the mean concentrations of the elements in Portuguese wines (Catarino et al. 2008) and to the maximum allowed values according to the Organization International de le Vigne et du Vin (OIV 2005). The chemical analysis of the three studied samples of arbutus berry brandy (one made with fruits collected on plants growing in the mine area and two made with fruits from plants growing out of the contaminated area) is presented in Table 6.
Although the high concentrations of Al in the majority of the arbutus berries fruits collected in Panasqueira (15–124 mg Al kg−1, Table 4) comparing to fruits sampled by Özcan and Haciseferoğullari (2007; 20.11 ± 2.69 mg Al kg−1) in a non-contaminated area, only one sample of the brandy (BAL 2 = 0.097 mg Al L−1, Table 6) exceeded the analytic parameter limit (dl < 0.05 mg L−1), which is lower than the mean concentration of the element in Portuguese wines (0.18–8.6 mg L−1, Catarino et al. 2008). This brandy sample also exceeded the analytic limit of iron (0.593 mg Fe L−1, Table 6), but not the mean content in Portuguese wines (0.24–19.40 mg Fe L−1, Catarino et al. 2008).
The three brandy samples had smaller As concentrations than the maximum allowed values for wines (0.2 mg L−1, OIV 2005), and Cd and W concentrations are lower than the analytical detection limit (0.05 mg kg−1 for both chemical elements) that is higher than the maximum allowed value for Cd in wines (0.01 mg Cd L−1, OIV 2005) and higher than the concentration of W in Portuguese wines (0.09–10.5 μg W L−1, Catarino et al. 2008). Concerning Cu concentration, the brandy samples did not exceed the limit defined in the Portuguese legislation (Decreto-Lei no. 238/2000) for arbutus berry brandy (15 mg Cu L−1).
Brandy samples distilled from berries collected on arbutus trees growing out of the contaminated area contain Pb and Zn whose concentrations exceeded the maximum allowed values for wines (0.15 mg Pb L−1 and 5.0 mg Zn L−1, OIV 2005). This is probably due to the equipment used in the distillation process by local private producers.
The majority of the analysed chemical elements in the arbutus berry brandy distilled from berries collected within the Panasqueira mine area (BAL 1) have concentrations lower than those in the two brandy samples distilled using berries collected on plants growing on non-contaminated soils (BAL 2 and BAL 3), showing that the high concentration of hazardous chemical elements in soils does not appear to have a negative impact on A. unedo fruits and on the distilled brandy.
Health risk from consumption of leaves and twigs, and fruits
Arbutus unedo has been widely used in traditional medicine, throughout the Mediterranean regions (Italy, Morocco and Turkey), with the employment of infusions and decoctions of almost all parts of this plant: leaves, twigs, fruits, barks and roots. Several potential benefits for human health have been reported by several authors for both leaves and fruits (Malheiro et al. 2012; Oliveira et al. 2011; and references therein). Potential uses of arbutus berries in food industry have also been suggested (fruit pieces in yoghurt, pie and pastry filling or cereal products) or as a food colorant, considering their content of β-carotene and anthocyanins (Alarcão-e-Silva et al. 2001).
It is therefore opportune to assess the health risk of A. unedo to the inhabitants of the Panasqueira area due to fruit consumption, either fresh or after processing, or to the use of arbutus leaves and twigs to make infusions. The HQs for the fruit were calculated for As, Cd, Cu and Zn, using Eq. (2) (Section 2.5), and the chemical exposure dose (EDing) (Eq. (1)) was estimated from the concentration (C) (maximum values) of the above-referred elements in the fruits (Table 4) together with the following assumptions: a body weight (W) of 76 kg for the average adult (Alves et al. 2006), an adult lifetime of 70 years (E d), that one person usually does not eat more than 4 kg of berries/year (0,011 kg of fruits a day) (F i) and that the normal fruits’ maturation period is around 4 months (120 days/year) (E f). The chemical exposure dose for the intake of an infusion made with leaves and twigs of A. unedo was calculated considering that 0.3 kg of leaves and twigs per year will be used for infusion, making a maximum of 96 days/year of infusion consumption.
The established value for the oral reference dose (RfD) of each chemical element as well as the respective calculated chemical exposure dose (EDing) together with the values of the HQ for the berries and for the leaves and twigs is shown in Table 7. The calculated HQ for each chemical element for an average inhabitant of the Panasqueira areas who uses the berries and the shoots for consumption is lower than unity (Table 7).
The results of this study indicate that the leaves and twigs, and fruits of arbutus tree growing on soils with high total and, in some cases, high available fraction concentrations of As, Cd, Cu and Zn probably do not constitute danger for human health risks during a lifetime. However, more risk assessments and studies have to be done for a more complete exclusion of any such risk.
Soils in the Panasqueira mining area, especially those developed on tailings and/or receiving the influence of seepage water from waste heaps or effluent from the mine water treatment plant, were contaminated with trace elements, mainly As, Cu, Pb, W and Zn. The elemental concentrations in the soil available fraction, extracted with DTPA, were quite variable. In the solutions of the soil available fraction, Cd and Zn were the elements that, in general, had the higher percentage of the total soil concentration, reaching a maximum of 76 % for Cd and 60 % for Zn.
The majority of the samples of the A. unedo shoots (leaves and twigs) showed concentrations of Al, Cu, Fe, Pb, Mn and Zn in the normal rage for plants in general; however, Cd concentrations exceeded the values considered tolerable for crops, but are lower than the toxic limit for cattle. Cadmium, W and Zn are preferentially translocated from the roots to shoots of A. unedo whereas Al, As, Cu, Fe and Pb are accumulated in the roots of this species.
The arbutus tree is part of the Beira Interior’s Forest Landscape Planning, as a species with great fire resistance and a good economic profit due to the use of arbutus berry to produce brandy. In fact, the analysis of the fruits collected in the A. unedo trees growing on the contaminated soils and the calculated hazard quotient for As, Cd, Cu and Zn allows the authors to conclude that the consumption of the arbutus berries probably does not constitute a risk for human health during a lifetime. Consequently, these fruits can be used to produce brandy and the brandy sample obtained by distillation of the berries collected within the mine area had Cu concentrations below the allowed limit according to the Portuguese legislation for arbutus berry brandy.
Arbutus unedo trees can be used in the phytostabilization programs in the Panasqueira area because it is one of the species that spontaneously colonizes the tailings, belonging to the group of plants of the first stages of vegetation development, promoting waste weathering and pedogenesis and decreasing water and wind erosion. In addition, this species is not an accumulator of trace elements and their concentrations in the above-ground part of the plants will not represent a threat for the biological systems.
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The authors would like to thank the Portuguese Foundation for Science and Technology (FCT) for the financial research support of CICECO (Program Pest-PEst-C/CTM/LA0011/2013) and Unidade de Investigação Química Ambiental (UIQA, Projecto Estratégico/528).
Responsible editor: Claudio Bini
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Abreu, M.M., Godinho, B. & Magalhães, M.C.F. Risk assessment of Arbutus unedo L. fruits from plants growing on contaminated soils in the Panasqueira mine area, Portugal. J Soils Sediments 14, 744–757 (2014). https://doi.org/10.1007/s11368-013-0835-7
- Arbutus berry brandy
- Health risks
- Mine soils
- Panasqueira mine