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Soil and plant contamination by lead mining in Bellmunt (Western Mediterranean Area)
Journal of Geochemical Exploration 113 (2012) 94–99
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Soil and plant contamination by lead mining in Bellmunt (Western Mediterranean Area) J. Bech a,⁎, N. Roca a, d, J. Barceló b, P. Duran a, P. Tume c, C. Poschenrieder b a
Soil Science Laboratory, Faculty of Biology, Universitat de Barcelona, Avda Diagonal 645, 08028 Barcelona, Spain Plant Physiology Laboratory, Bioscience Faculty, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain Facultad de Ingeniería. Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile d Faculty of Agronomy, Universidad Nacional del Centro de la Provincia de Buenos Aires, CC 47, 7300 Azul, Argentina b c
a r t i c l e
i n f o
Article history: Received 15 October 2010 Accepted 4 October 2011 Available online 12 October 2011 Keywords: Lead Mining activity Moricandia moricandioides Soil pollution Zinc Zinc accumulator
a b s t r a c t Galena has been mined in Bellmunt (Priorat, Western Mediterranean Area) since ancient times until 1972. While sediment pollution originated by the mining activity in the Ebro River passing the region has been investigated to some extent, the local impact on soils and plants has received poor attention. Here we report first results on the concentrations of major metal contaminants and antimony in soils and representative plants from four selected sites with different pollutant burdens around the mining area. Total (HNO3, HF digest) soil concentrations were analysed. Soils had alkaline pH (8.0 ± 0.2), organic matter contents ranging from 8 to 24 g kg− 1, and a sandy-loam or a loamy-sand texture. Present study highlighted that metal accumulation in different plants varied with species, tissues and metals. All analysed plant species showed enhanced root and shoot concentrations of Cu, Pb, Zn, and Sb when growing on the more polluted soils and all, but one, restricted the translocation of metals from roots to shoots exhibiting shoot/root concentration ratios lower or close to unity. A notably exception was Moricandia moricandioides (Boiss.) Heyw. [M. ramburii Webb] where shoot/root Zn concentration ratios up 5.5 were observed. This metal accumulation pattern was only observed for Zn and not for other analysed metal contaminants. The concentrations of other, poorly mobile metals, like Pb or Cu were always higher in roots than in shoots (e.g. Pb shoot/root ratios ranged from 0.13 to 0.24). Taking into account the high Pb burden of the soil samples and these low shoot/root Pb ratios, it can be excluded that the particular Zn accumulation pattern of M. moricandioides was biased by soil contamination of shoot samples. To our best knowledge this is the first report of Zn accumulation behaviour in a Moricandia species. The soil-to-shoot transfer factors (SAF) for this species were, however, relatively low ranging from 0.2 to 1.3. Further studies are required to confirm the possible Zn-accumulator character of M. moricandioides. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Galena mining has occurred in Spain for several thousands of years (Leblanc et al., 2000). The consequent pollution of sediments and soils has received attention especially in the highly acidic area of the large Pyrite Belt in the south-western part of the Iberian Peninsula (Ruíz et al., 2008; Velasco et al., 2005). Much less information is available concerning the environmental impact of the, ancient lead mines in Catalonia, the North-Eastern part of the Iberian Peninsula. Here, several small abandoned lead mines are scattered along the Western Mediterranean coastal area (Mata Perelló, 1990). The most important galena veins are located in Bellmunt (Priorat) where galena was extracted from ancient times up until 1972.
⁎ Corresponding author. E-mail address: [email protected] (J. Bech). 0375-6742/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.gexplo.2011.10.001
While in this region sediment pollution originated by the mining activity in the Ebro River has been investigated (Ferré, 2007), the local impact on soils and plants has received little attention. Due to the fact that at Bellmunt mine soils have high pH and large carbonate concentrations, investigations on uptake and translocation of trace elements by the natural vegetation are not limited to local interest, but also of a broader significance. Soil pH affects not only metal availability, but also many processes of metal uptake by plants though this effect appears to be metal specific (Brown et al., 1995). Relatively small amounts of data on metal uptake by natural vegetation in neutral to alkaline soils with high metal burdens are available (CarrilloGonzález and González-Chávez, 2006; Conesa et al., 2006; Grodzinska et al., 2010; Poschenrieder et al., 2001; Szarek-Lukaszewska and Niklinska, 2002; Wang et al., 2008). This contrasts with the more widely described mine spoil sites where moderate to extreme acidity is an important factor influencing metal availability and phytotoxicity (Ernst, 1974; Rufo and de la Fuente, 2010). Investigations on the natural vegetation simultaneously adapted to high soil carbonate and
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high metal availability can be important for both the fundamental knowledge on metal uptake and tolerance mechanisms and for the characterization of germplasm for phytoremediation of large areas of near neutral to alkaline mine spoils (McCabe and Otte, 2000; Schroeder et al., 2005). Therefore, the objectives of this study were 1) to determine the total contents of selected heavy metals (Cd, Pb, Sb and Zn) in soils and plants collected around tailings of an old lead mine and 2) to assess the tolerance strategies developed by the natural vegetation at this site in order to evaluate their potential for phytoremediation purposes. 2. Materials and methods 2.1. Site description and collection of samples The Eugenia mine is located at a height of 261 m above sea level in Bellmunt (Priorat), an ancient mining village at 30 km West of Tarragona, Catalonia (NE Spain). The UTM coordinates are: X 312.700 and Y 4.559.575. The study area at Bellmunt is situated in the Mora tectonic depression limited by two faults in NE–SW direction. This depression is located in the South of the Catalonian Pre-coastal Range. Geologically, the bedrock consists of metamorphic dark schists of Silurian and Carboniferous age, affected by the Hercynian and Alpine orogenies. The folds' orientation mainly are NW–SE, Armorican direction. In the neighborhood areas quartzitic porphyry dikes and outcrops of granitic aureoles occur. Metamorphic schists are rich in oligoclase, quartz and dolomite and the porphyries are rich in quartz. The most frequent minerals are: Galena (PbS), Sphalerite (ZnS), Cerusite (PbCO3), Baritine (BaSO4), Silver (Ag), Pyrite (FeS2), Chalcopyrite (CuFeS2), Dolomite (CaCO3MgCO3), and Calcite (CaCO3). The mine has been in use since ancient times, and consists of 14 km of galleries and has a depth of 600 m. Mining activity finished in 1972, leaving waste piles of mine spoils with a thickness of up to 50 m. Four sampling sites (S1 to S4) with different degrees of contamination, as assessed by their visual aspect, were chosen according to the following selection criteria: vegetation cover, distance from the ore processing facility, predominant direction of wind, and the longitudinal sequence in relation to a gradient of metal concentrations. At each site, a representative volume per soil samples (0–20 cm depth) was taken from apparently low (S1) to high (S4) pollution levels, and 2 kg sub-sample of sample was taken back to laboratory for sample preparation and analysis. Plant samples were collected from the same sites as the soil samples. At least two to four individuals of all plant species were randomly collected within the sampling areas. Besides the Brassicaceae species Moricandia moricandioides (Boiss.) Heyw. [M. ramburii Webb] that was present at all sites (S1, S2, S3 and S4), two Asteraceae species, Sonchus tenerrimus L. (sites S1, S2 and S3) and Crepis vesicaria L. (site S2), one Plantaginaceae species Plantago amplexicaulis L. (sites S1, S3 and S4) and one Papaveracean species, Glaucium flavum Crantz (site 2) were considered.
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To determine the total soil metal concentrations air dried and sieved samples were ground to a fine powder using an agate ball mill. A subsample of 0.1 g mixed with 2.5 ml of HNO3 and 2.5 ml of water was heated at 90 °C for 3 h in closed vessels. The extract was centrifuged and transferred to a volumetric flask. The residue was transferred to Teflon vessel with 5 ml HF and 2 ml HNO3, keeping it at 90 °C overnight. The extract was transferred to another Teflon vessel with 2 ml HClO4 and the residue was heated again with 5 ml HCl at 90 °C for 2 h. All extracts were transferred to the second Teflon vessel with 2 ml HClO4 and then, evaporated. To the final residue 5 ml of water and 2.5 ml of HNO3 were added and then heated to boil. Finally, it was transferred to the volumetric flask. Metal analysis in the extracts was determined by inductively coupled plasma-mass spectrometer (ICP-MS Perking Elmer Elaw 6000). After immediate transfer to the laboratory plant samples were separated into roots and shoots. The plant material was carefully washed with tap water followed by distilled water. The oven dried (60 °C) plant material was digested in a microwave oven using a mixture (5:1) of HNO3 (65%), H2O2 (30%) in closed vessels. Potentially toxic trace elements in the plant digests were analysed by ICP-ES (Jobin Yvon-VHR 38). Quality control was assured by the use of duplicate analyses performed on all samples, the use of reagent blanks, and a standard reference soil (CRM 141 R, BCR, Brussels), whose analysis yielded Cr, Ni and Cu contents close to the certified values. The average precision was better than 10%. The detection limits for the metals in mg kg − 1 were: Cd (0.1), Cu (0.1), Pb (0.1), Sb (0.07) and Zn (0.8). 2.3. Statistical analysis The data is presented as mean and ±standard deviation. Shoot accumulation factor (SAF) is defined as the ratio of metal concentration in shoots to that in soil which is a measure of the ability of a plant uptake and transport metals to the shoots (Vyslouzilova et al., 2003). The translocation factor (TF) is defined as the ratio of metal concentration in the plant shoot to that in the root (Sun et al., 2008). One way ANOVA was carried out to compare the difference of means from various sampling sites, followed by Bonferroni multiple comparison test (p b 0.05). All statistical evaluations were performed using the SPSS software package (SPSS, 2000). 3. Results and discussion 3.1. Soil properties The physico-chemical properties of the soils of all sampling sites are presented in Table 1. The soils sampled around the galena mine had quite similar physico-chemical properties. At all sampling sites soils had basic pH and no salinity problem according to the values of electrical conductivity. Soils were characterized by high calcium carbonate concentrations, organic matter content between 13 and
2.2. Soil and plant analysis The collected soil samples were transferred to the laboratory, air dried and then sieved through a 2 mm screen. The b 2 mm fraction of the soil samples were stored in paper bags, in dark, dry conditions, at room temperature, for subsequent analysis. The pipette method was used to determine particle size distribution in the soil samples (b2 mm). Soil pH was measured potentiometrically in water at soil-to-solution ratio of 1:2.5 (MAPA, 1994). Organic carbon (OC) content was determined using the Walkley– Black dichromate acid oxidation method. Electrical conductivity (EC) in 1:5 (soil:water) solution was determined by potentiometry and CaCO3 by dissolution with HCl and titration of its excess with NaOH.
Table 1 Selected physico-chemical properties of soils sampled around the Eugenia galena mine in Bellmunt, mean and standard deviation with n = 2 (EC, electrical conductivity; OM, organic matter).
pHw pHKCl EC (dS cm− 1) CaCO3 (g kg− 1) OM (g kg− 1) Sand (%) Silt (%) Clay (%) Texture classes
S1
S2
S3
S4
8.2 ± 0.1 7.3 ± 0.1 0.3 ± 0.1 184 ± 13 24.0 ± 0.3 66.4 ± 2.3 17.2 ± 0.8 16.4 ± 0.3 Sandy loam
7.8 ± 0.2 7.5 ± 0.1 1.2 ± 0.1 277 ± 35 14.0 ± 1.4 79.8 ± 5.4 9.6 ± 4.3 10.5 ± 1.1 Sandy loam
7.8 ± 0.1 7.4 ± 0.1 1.8 ± 0.3 292 ± 18 13.0 ± 1.4 67.8 ± 2.5 21.0 ± 3.4 11.2 ± 0.8 Sandy loam
8.0 ± 0.1 7.6 ± 0.2 1.3 ± 0.2 337 ± 21 14.0 ± 0.9 84.1 ± 2.5 7.7 ± 1.4 8.2 ± 0.5 Loamy sand
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Table 2 Mean total (HF/HNO3 digest) concentrations (mg kg− 1 air dry soil) and standard deviation (n=3) of selected trace elements in soils around the Eugenia galena mine at Bellmunt (Priorat). For any given element, within a row, values followed by the same letter do not differ at p= 0.05.
CuT PbT SbT ZnT
S1
S2
S3
S4
89.3 ± 7.7a 19358 ± 347a 9.7 ± 0.2a 318 ± 5.1a
257 ± 48a 28998 ± 378b 19.5 ± 0.7b 837 ± 96b
387 ± 15.7a 37197 ± 210c 24.5 ± 0.6c 749 ± 4.6b
415 ± 39.4a 38956 ± 356d 31.1 ± 0.6d 989 ± 39.1 b
Table 4 Concentrations and standard deviation of selected trace elements (μg g− 1 dry weight) in shoots (S) and roots (R) of C. vesicaria (n = 4) and G. flavum (n = 2) that only grow at moderate pollution site (S2). Species
Organ
Cu
Pb
Sb
Zn
C. vesicaria
S R S R
15.1 ± 5.3 32.4 ± 21.8 11.2 ± 1.0 60.8 ± 21.7
369 ± 125 1815 ± 265 121 ± 50.3 6968 ± 1187
0.7 ± 0.5 1.1 ± 0.2 0.4 ± 0.0 2.5 ± 0.2
107 ± 30.0 92.6 ± 13.4 114 ± 50.5 379 ± 157
G. flavum
3.3. Plant elemental composition 24 g kg − 1, and a sandy-loam or a loamy sand texture. The local reference topsoil samples (S1) presented the greatest pH (i.e., pH = 8.1) with the smallest calcium carbonate content. 3.2. Soil elemental composition The concentration of heavy metals and metalloids varied greatly (Table 2). Soils from sampling sites S1 and S4 had the smallest and the largest contamination burdens, respectively. All soil samples contained high concentrations of Pb, Zn, Cu and Sb. As expected, the most abundant metal pollutant was Pb, reaching 3.9% in soils of site S4. The total Pb content exceeded the ranges that are considered toxic to normal plants. In soils with a pH greater than 7.0, the established threshold value for agricultural use is 300 mg kg − 1 (BOE, 1990). Similar values were cited by Bernal et al. (2007), and Bowen (1979), while Kabata-Pendias and Mukherjee (2007) and Sheppard et al. (1992) suggested values of 400 mg kg − 1 and 750 mg kg − 1, respectively. The soil metal concentrations found in this study at Bellmunt are higher than those usually reported for superfund sites (Gasser et al., 1996; Pichtel et al., 2001). Zinc was the second most abundant soil contaminant around the mine followed by Cu. However, the concentrations of Zn in Bellmunt mine soils were smaller than those contained in the literature for other sites; e.g. the Monica mine in Spain reported a total Zn concentration of 846 mg kg − 1 or Andacollo mining zone in Northern Chile with 480 mg kg − 1 (Higueras et al., 2004). Soil Sb concentrations were enhanced in relation to local reference topsoil samples (S1), but clearly below the extreme levels reported in the vicinity of smelters (Edwards et al., 1995).
A total of five plant species were investigated for heavy metal concentrations in their tissues as these species were dominating the studied sites (Tables 3 and 4). Metal concentrations in the studied plants were very variable. The greatest shoot Cu, Pb and Sb concentrations were observed in Plantago amplexicaulis (Table 3). However, the greatest Zn shoot concentrations were observed in Moricandia moricandioides. The maximum root metal and Sb concentrations were also found in P. amplexicaulis but always at the most polluted site (S4). It is well-known that another Plantago species, P. lanceolata can adapt to a large diversity of metal-rich habitats because of its potential for fast evolution of tolerance to Zn, As, Cu, and/or Pb (Pollard, 1980). P. lanceolata is widely distributed and has been proposed as a bioindicator for Pb, Zn, and Cd (Dimitrova and Yurukova, 2005). In contrast, P. Amplexicaulis is a therophyte species that is typically found in calcareous maritime soils of the Southern Mediterranean area, in the deserts of Egypt and Israel, and in the Arabian Peninsula (USDA, ARS, 2010). In Spain, P. amplexicaulis is located mainly in the South, in Almeria and Murcia, and can extend up to Castellón (Crespo et al., 2007; de la Torre et al., 1995). In the present study this species was found even further North. Probably the ability to tolerate both draught on the sandy, badly structured soils and high metal content allowed P. amplexicaulis to efficiently compete in the mine soil habitat located in this more Northern region. Glaucium flavum, a species of the Papaveraceae family, typically from calcareous, well-drained marine habitats of the Mediterranean region was only found at site S2 with somewhat lower metal burdens than the other soil with great sand content from site S4. The minimum
Table 3 Concentrations and standard deviation of selected trace elements (μg g− 1 dry weight) in shoots (S) and roots (R) of M. moricandioides (n = 2 at S1, S3 and S4 and n = 4 at S2). P. amplexicaule (n = 2) and S. tenerrimus (n = 2) that only grow at three of the four sampling sites. For any given element, within a row, values followed by the same letter do not differ at p = 0.05. Species
Organ
TE
S1
S2
S3
S4
M. moricandioides
S
Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn
10.3 ± 0.7a 238 ± 19.6a 0.29 ± 0.01a 426 ± 83.7a 11.6 ± 3.0a 1026 ± 569ab 0.66 ± 0.27a 75.7 ± 8.7a 24.3 ± 2.4a 417 ± 37a 1.83 ± 2.21a 257 ± 24a 27.3 ± 5.2a 3996 ± 1071a 1.56 ± 0.10a 155 ± 37a 12.5 ± 5.0a 138 ± 11a 1.21 ± 0.02a 86 ± 1a 29.7 ± 7.4a 4536 ± 659a 3.35 ± 0.69a 128 ± 21a
9.9 ± 2.0a 315 ± 145a 0.52 ± 0.16a 211 ± 19a 12.6 ± 4.4a 1334 ± 511a 1.15 ± 0.23a 59.2 ± 20.0a
6.7 ± 0.1a 550 ± 45a 0.78 ± 0.07a 136 ± 46a 32.3 ± 11.8ab 4417 ± 550bc 3.22 ± 0.30ab 118 ± 9.3ab 39.9 ± 1.4b 7058 ± 293b 3.49 ± 0.16a 314 ± 15a 38.2 ± 13.2a 7705 ± 1175a 3.43 ± 1.19ab 399 ± 19a
27.3 ± 2.3b 1239 ± 263b 1.54 ± 0.34b 879 ± 247b 40.6 ± 9.6b 6209 ± 1815 c 5.33 ± 1.54b 223 ± 56b 19.1 ± 0.3a 1766 ± 85 c 1.25 ± 0.02a 309 ± 16a 119 ± 35.0a 16790 ± 5427a 7.15 ± 1.35b 771 ± 102b 39.5 ± 1.8b 610 ± 134a 1.10 ± 0.46a 312 ± 58a 36.9 ± 1.8a 4005 ± 16a 2.99 ± 0.45a 207 ± 27a
R
P. amplexicaulis
S
R
S. tenerrimus
S
R
34.3 ± 5.1b 620 ± 308a 2.64 ± 0.21b 169 ± 60a 86.0 ± 32.7a 9361 ± 4824a 5.80 ± 1.99a 356 ± 129a
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shoot Pb concentration was observed in G. flavum (Table 4). The most interesting species, however, was M. moricandioides. This Brassicaceae was found at all sampling sites and at all sites the shoot Zn concentrations exceeded those of roots (Table 3). Among all the plant species studied, no one was close to the minimum concentration criteria for considering a hyperaccumulator plant (100 mg kg − 1 in the case of Sb, 1000 mg kg − 1 in the case of Cu and Pb and, 10,000 mg kg − 1 for Zn) (Baker and Brooks, 1989; Brooks, 1998; Cluis, 2004). However, all the investigated plant species collected found to be tolerant to high metal concentrations with excellent adaptation to calcareous soils. 3.4. Phytoaccumulation and translocation in plants Plant's potential for phytoextraction can be estimated by both translocation factor (TF) and shoot accumulation factor (SAF). Plant species exhibiting TF and SAF greater than one are suitable for phytoextraction (Pilon-Smits, 2005). In the present study the SAF values were generally smaller than unity (Fig. 1). Only M. moricandioides had
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Zn shoot accumulation factor greater than one at the reference site (S1). The small SAF values are, in part, due to both the high metal burdens of the mine soils and the fact that here the total and not the pseudototal or extractable soil metal concentration were used for SAF calculation. The TF index revealed clear differences in the root to shoot translocation of Sb and heavy metals (Fig. 2). Among all the plants screened, P. amplexicaulis had highest TF for Cu, Pb and Sb. S. tenerrimus also showed a TF greater than one for Cu in S4. However the most significant results were observed for Zn. Four plant species i.e. M. moricandioides, S. tenerrimus, C. vesicaria and P. amplexicaulis, had a TF greater than one (Fig. 2). M. moricandioides was the only studied plant that showed efficient Zn translocation at all sites (S1, S2, S3 and S4). On all sampling sites, except S3, the shoot Zn concentrations of this species were at least three times higher than those of the roots. At the sampling site with the smallest soil Zn concentration (S1) the TF index for this chemical element even exceeded the value of 5 for M. moricandioides. Reports on high shoot/root metal ratios from field-sampled plant material have to be considered with caution because frequently contamination of the
Fig. 1. Shoot accumulation factor (SAF) of all the plant species collected around the galena mine of Bellmunt.
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Fig. 2. Translocation factor (TF) of all the plant species collected around the galena mine of Bellmunt.
leaves with soil particles cannot be excluded. In the M. moricandioides samples of the present study this was not the case. The soils contained much higher Pb than Zn concentrations. If soil particles would have been present in the shoot samples, a high Pb shoot/root ratio should have been observed. Actually, the Pb shoot/root ratios found in M. moricandioides in any case exceeded the value of 0.2. G. flavum, the species with a great root Pb concentration at site S2, was the most efficient shoot excluder of Pb, exhibiting a shoot to root ratio of only 0.02. Shoot/ root ratios for the other analysed trace elements, Cu, Zn, and Sb, were also small in G. flavum. A possible Zn-accumulation pattern in M. moricandioides was suggested. The great TF values for Zn observed in M. moricandioides are typically found in Zn hyperaccumulating Brassicaceae species such as Thlaspi caerulescens L. (Roosens et al., 2003; Tolrà et al., 1996). However, M. moricandioides should not be considered a Zn-hyperaccumulator as the shoot concentrations did not exceed 900 μg g− 1 dry weight (Table 3), a concentration that is considerably lower than the more than 10,000 μg g− 1 dry weight reported in T. caerulescens (Baker,
1981). This relatively low uptake of Zn could be due to the relatively high pH of the soils which can considerably hamper Zn bioavailability. M. moricandioides has been cited among wild Brassicaceae of interest, because it could be a valuable source of traits related to tolerance to calcareous soils and as a cover crop (Warwick et al., 2009). To our best knowledge this is the first report on possible Zn-accumulating character of M. moricandioides. 4. Conclusions The Bellmunt mining area offers singular conditions for the selection of germplasm that combines tolerance to high metal concentrations, especially Pb and Zn, with excellent adaptation to calcareous soils and draught. These plant species does not meet all the criteria of a hyperaccumulator, but none the less accumulated significant amounts of heavy metals in their tissues. Among the metal resistant plant species able to grow at the Bellmunt mine spoils the most contrasting behaviours were observed in G. flavum and in M. moricandioides. The accumulation
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strategy allowed M. moricandioides to colonize even the most polluted sites. Studies on metal uptake under controlled environmental conditions should be performed in order to characterize the mechanisms underlying the Zn-accumulation pattern in M. moricandioides. Acknowledgements The financial support from the Spanish Ministry of Science and Innovation is gratefully acknowledged (projects BFU2004-02237CO2-01 and BFU2007-60332/BFI). References Baker, A.J.M., 1981. Accumulators and excluders strategies in the response of plants to heavy metals. Journal of Plant Nutrition 3, 643–654. Baker, A.J.M., Brooks, R.R., 1989. Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1, 811–826. Bernal, M.P., Clemente, R., Vasquez, S., Walker, D.J., 2007. Aplicación de la Fitorremediación a los suelos contaminados por Metales Pesados en Aznalcóllar. Ecosistemas 2, 68–82. BOE, 1990. Real Decreto 1310/1990 Regulación de la utilización de los lodos de depuración en el sector agrario, in: BOE nº 262 (01/11/1990). Ministerio de Agricultura, Pesca y Alimentación, Spain, pp. 32339–32340. Bowen, H.J.M., 1979. Environmental Chemistry of the Elements. Press, New York. Brooks, R.R., 1998. Geobotany and hyperaccumulators. In: Brooks, R.R. (Ed.), Plants that Hyperaccumulate Heavy Metals. Their Role in Phytoremediation, Microbiology, Archaeology, Mineral Exploration and Phytomining. Cab International, United Kingdom, pp. 54–94. Brown, S.L., Chaney, R.L., Angle, J.S., Baker, A.J.M., 1995. Zinc and cadmium uptake by hypeaccumulator Thlaspi caerulescens and metal tolerant Silene vulgaris grown on sludge amended soils. Environmental Science & Technology 29, 1581–1585. Carrillo-González, R., González-Chávez, M.C.A., 2006. Metal accumulation in wild plants surrounding mining wastes. Environmental Pollution 144, 84–92. Cluis, C., 2004. Junk-greedy greens: phytoremediation as a new option for soil decontamination. Journal of Biotechnology 2, 60–67. Conesa, H.M., Faz, A., Amaldos, R., 2006. Heavy metal accumulation and tolerance in plants from mine tailings of the semiarid Cartagena-La Unión mining district (SE Spain). The Science of the Total Environment 366, 1–11. Crespo, M.B., Alonso, M.A., Camuñas, E., Juan, A., Martínez Azorín, M., 2007. Plantago amplexicaulis CAV. (Plantaginaceae) en la Provincia de Castellón. Flora Montiberica 35, 24–27. De la Torre, A., Vicedo, M., Alonso, M.A., 1995. Flora y vegetación de algunas islas de Alicante (SE España). Ecologia Mediterranea 21, 113–128. Dimitrova, I., Yurukova, L., 2005. Bioindication of anthropogenic pollution with Plantago lanceolata (Plantaginaceae): metal accumulation, morphological and stomatal leaf characteristics. Phytologia Balcanica 11, 89–96. Edwards, R., Lepp, N.W., Jones, K.C., 1995. Other less abundant elements of potential environmental significance: antimony, In: Alloway, B.J. (Ed.), Heavy Metals in Soils, 2nd ed. . ISBN: 0751401986, pp. 306–352. Ernst, W.H.O., 1974. Schwermetallvegetation der Erde. Gustav Fischer Verlag, Stuttgart343730187X. Ferré, N., 2007. Nivells de metals pesants a la conca Catalana del riu Ebre. Avaluació del risc per la población i l'ecosistema. Universitat Rovira Virgili. 978-84-691-0371-5. Gasser, U.G., Walker, W.J., Dahlgren, R.A., Borch, R.S., Burau, R.G., 1996. Lead release from smelter and mine waste impacted materials under simulated gastric conditions and relation to speciation. Environmental Science & Technology 30, 761–769. Grodzinska, K., Szarek-Lukaszewska, G., Godzik, B., 2010. Pine forest of Zn–Pb post-mining areas of Southern Poland. Polish Botanical Journal 55, 229–237. Higueras, P., Oyarzun, R., Oyarzún, J., Maturana, H., Lillo, J., Morata, D., 2004. Environmental assessment of copper–gold mercury mining in the Andacollo y Punitaqui districts, northern Chile. Applied Geochemistry 19 (11), 1855–1864.
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Kabata-Pendias, A., Mukherjee, A.B., 2007. Trace Elements from Soil to Human. Springer. Leblanc, M., Morales, J.A., Borrego, J., Elbaz-Poulichet, F., 2000. 4,500-year-old mining pollution in Southwestern Spain: long-term implications for modern mining pollution. Economic Geology 95, 655–662. MAPA, 1994. Official Methods for soils and water analysis. Spanish Ministry of Agriculture, Fishing and Food, Madrid, Spain. Mata Perelló, J.M., 1990. Els Minerals de Catalunya. Institut d'Estudis Catalans, Barcelona8472831477. McCabe, O.M., Otte, M.L., 2000. The wetland grass Glyceria fluitans for revegetation of mine tailings. Wetlands 20, 548–559. Pichtel, J., Vine, B., Kuula-Väisänen, Niskanen, P., 2001. Lead extraction from soils as affected by lead chemical and mineral forms. Environmental Engineering Science 18, 91–98. Pilon-Smits, E., 2005. Phytoremediation. Annual Review of Plant Biology 56, 15–39. Pollard, A.J., 1980. Diversity of metal tolerances in Plantago lanceolata L. from the Southeastern United States. New Phytologist 86, 109–117. Poschenrieder, C., Bech, J., Llugany, M., Pace, A., Fenés, E., Barceló, J., 2001. Copper in plant species in a copper gradient in Catalonia (North East Spain) and their potential for phytoremediation. Plant and Soil 230, 247–256. Roosens, N., Verbruggen, N., Meerts, P., Ximénez-Embún, P., Smith, J.A.C., 2003. Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant, Cell & Environment 26, 1657–1672. Rufo, L., de la Fuente, V., 2010. Sucessional dynamics of the climatophile vegetation of the mining territory of the Rio Tinto Basin (Huelva, Spain): soil characteristics and implications for phytoremediation. Arid Land Reserach and Management 24, 301–327. Ruíz, F., Borrego, J., González-Regalado, M.L., López González, N., Garro, B., Abad, M., 2008. Impact of millenial mining activities on sediments and microfauna of the Tinto River estuary (SW Spain). Marine Pollution Bulletin 56, 1258–1264. Schroeder, K., Rufaut, C.G., Smith, C., Mains, D., Craw, D., 2005. Rapid plant-cover establishment on gold mine tailings in Southern New Zealand: glasshouse screening trials. International Journal of Phytoremediation 7, 307–322. Sheppard, S.C., Gauded, C., Sheppar, P.I., Cureton, P.M., Wong, M.P., 1992. The development of assessment and remediation guidelines for contaminated soils: a review of the science. Canadian Journal of Soil Science 72, 259–394. SPSS, 2000. User Manual. SPSS Inc., Chicago, IL. Sun, Y., Zhou, Q., Diao, C.H., 2008. Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Bioresource Technology 99, 1103–1110. Szarek-Lukaszewska, G., Niklinska, M., 2002. Concentration of alkaline and heavy metals in Biscutella laevigata L and Plantago lanceolata L. growing on calamine spoils (S. Poland). Acta Biologica Cracoviense Series Botanica 44, 29–38. Tolrà, R.P., Poschenrieder, C., Barceló, J., 1996. Zinc hyperaccumulation in Thlaspi caerulescens. I. Influence on growth and mineral nutrition. Journal of Plant Nutrition 19, 1531–1540. USDA, ARS, 2010. National Genetic Resources Program. Germplasm Resources Information Network - (GRIN) [Online Database].National Germplasm Resources Laboratory, Beltsville, Maryland. http://www.ars-grin.gov/cgi-in/npgs/html/taxon.pl?28779. (14 October 2010). Velasco, F., Alvaro, A., Suarez, S., Herrero, J.M., Yusta, I., 2005. Mapping Fe-bearing hydrated sulphate minerals with short wave infrared (SWIR) spectral analysis at San Miguel mine environment, Iberian Pyrite belt (SW Spain). Journal of Geochemical Exploration 87, 45–72. Vyslouzilova, M., Tlustos, O., Szakova, J., Pablicova, D., 2003. As, Cd, Pb and Zn uptake by different Salix spp. grown at soils enriched by high loads of these elements. Plant, Soil and Environment 49 (5), 191–196. Wang, X., Liu, Y., Zeng, G., Chai, L., Xiao, X., Song, X., Min, Z., 2008. Pedological characteristics of Mn mine tailings and metal accumulation by native plants. Chemosphere 72, 1260–1266. Warwick, S.I., Francis, A., Gugel, R.K., 2009. Guide to wild germplasm of Brassica and allied crops (tribe Brassicaceae, Brassicaceae), 3rd edition. Brassica.info http://www. brassica.info/info/publications/guide-wild-germplasm.php.
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Soil and plant contamination by lead mining in Bellmunt (Western Mediterranean Area) J. Bech a,⁎, N. Roca a, d, J. Barceló b, P. Duran a, P. Tume c, C. Poschenrieder b a
Soil Science Laboratory, Faculty of Biology, Universitat de Barcelona, Avda Diagonal 645, 08028 Barcelona, Spain Plant Physiology Laboratory, Bioscience Faculty, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain Facultad de Ingeniería. Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile d Faculty of Agronomy, Universidad Nacional del Centro de la Provincia de Buenos Aires, CC 47, 7300 Azul, Argentina b c
a r t i c l e
i n f o
Article history: Received 15 October 2010 Accepted 4 October 2011 Available online 12 October 2011 Keywords: Lead Mining activity Moricandia moricandioides Soil pollution Zinc Zinc accumulator
a b s t r a c t Galena has been mined in Bellmunt (Priorat, Western Mediterranean Area) since ancient times until 1972. While sediment pollution originated by the mining activity in the Ebro River passing the region has been investigated to some extent, the local impact on soils and plants has received poor attention. Here we report first results on the concentrations of major metal contaminants and antimony in soils and representative plants from four selected sites with different pollutant burdens around the mining area. Total (HNO3, HF digest) soil concentrations were analysed. Soils had alkaline pH (8.0 ± 0.2), organic matter contents ranging from 8 to 24 g kg− 1, and a sandy-loam or a loamy-sand texture. Present study highlighted that metal accumulation in different plants varied with species, tissues and metals. All analysed plant species showed enhanced root and shoot concentrations of Cu, Pb, Zn, and Sb when growing on the more polluted soils and all, but one, restricted the translocation of metals from roots to shoots exhibiting shoot/root concentration ratios lower or close to unity. A notably exception was Moricandia moricandioides (Boiss.) Heyw. [M. ramburii Webb] where shoot/root Zn concentration ratios up 5.5 were observed. This metal accumulation pattern was only observed for Zn and not for other analysed metal contaminants. The concentrations of other, poorly mobile metals, like Pb or Cu were always higher in roots than in shoots (e.g. Pb shoot/root ratios ranged from 0.13 to 0.24). Taking into account the high Pb burden of the soil samples and these low shoot/root Pb ratios, it can be excluded that the particular Zn accumulation pattern of M. moricandioides was biased by soil contamination of shoot samples. To our best knowledge this is the first report of Zn accumulation behaviour in a Moricandia species. The soil-to-shoot transfer factors (SAF) for this species were, however, relatively low ranging from 0.2 to 1.3. Further studies are required to confirm the possible Zn-accumulator character of M. moricandioides. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Galena mining has occurred in Spain for several thousands of years (Leblanc et al., 2000). The consequent pollution of sediments and soils has received attention especially in the highly acidic area of the large Pyrite Belt in the south-western part of the Iberian Peninsula (Ruíz et al., 2008; Velasco et al., 2005). Much less information is available concerning the environmental impact of the, ancient lead mines in Catalonia, the North-Eastern part of the Iberian Peninsula. Here, several small abandoned lead mines are scattered along the Western Mediterranean coastal area (Mata Perelló, 1990). The most important galena veins are located in Bellmunt (Priorat) where galena was extracted from ancient times up until 1972.
⁎ Corresponding author. E-mail address: [email protected] (J. Bech). 0375-6742/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.gexplo.2011.10.001
While in this region sediment pollution originated by the mining activity in the Ebro River has been investigated (Ferré, 2007), the local impact on soils and plants has received little attention. Due to the fact that at Bellmunt mine soils have high pH and large carbonate concentrations, investigations on uptake and translocation of trace elements by the natural vegetation are not limited to local interest, but also of a broader significance. Soil pH affects not only metal availability, but also many processes of metal uptake by plants though this effect appears to be metal specific (Brown et al., 1995). Relatively small amounts of data on metal uptake by natural vegetation in neutral to alkaline soils with high metal burdens are available (CarrilloGonzález and González-Chávez, 2006; Conesa et al., 2006; Grodzinska et al., 2010; Poschenrieder et al., 2001; Szarek-Lukaszewska and Niklinska, 2002; Wang et al., 2008). This contrasts with the more widely described mine spoil sites where moderate to extreme acidity is an important factor influencing metal availability and phytotoxicity (Ernst, 1974; Rufo and de la Fuente, 2010). Investigations on the natural vegetation simultaneously adapted to high soil carbonate and
J. Bech et al. / Journal of Geochemical Exploration 113 (2012) 94–99
high metal availability can be important for both the fundamental knowledge on metal uptake and tolerance mechanisms and for the characterization of germplasm for phytoremediation of large areas of near neutral to alkaline mine spoils (McCabe and Otte, 2000; Schroeder et al., 2005). Therefore, the objectives of this study were 1) to determine the total contents of selected heavy metals (Cd, Pb, Sb and Zn) in soils and plants collected around tailings of an old lead mine and 2) to assess the tolerance strategies developed by the natural vegetation at this site in order to evaluate their potential for phytoremediation purposes. 2. Materials and methods 2.1. Site description and collection of samples The Eugenia mine is located at a height of 261 m above sea level in Bellmunt (Priorat), an ancient mining village at 30 km West of Tarragona, Catalonia (NE Spain). The UTM coordinates are: X 312.700 and Y 4.559.575. The study area at Bellmunt is situated in the Mora tectonic depression limited by two faults in NE–SW direction. This depression is located in the South of the Catalonian Pre-coastal Range. Geologically, the bedrock consists of metamorphic dark schists of Silurian and Carboniferous age, affected by the Hercynian and Alpine orogenies. The folds' orientation mainly are NW–SE, Armorican direction. In the neighborhood areas quartzitic porphyry dikes and outcrops of granitic aureoles occur. Metamorphic schists are rich in oligoclase, quartz and dolomite and the porphyries are rich in quartz. The most frequent minerals are: Galena (PbS), Sphalerite (ZnS), Cerusite (PbCO3), Baritine (BaSO4), Silver (Ag), Pyrite (FeS2), Chalcopyrite (CuFeS2), Dolomite (CaCO3MgCO3), and Calcite (CaCO3). The mine has been in use since ancient times, and consists of 14 km of galleries and has a depth of 600 m. Mining activity finished in 1972, leaving waste piles of mine spoils with a thickness of up to 50 m. Four sampling sites (S1 to S4) with different degrees of contamination, as assessed by their visual aspect, were chosen according to the following selection criteria: vegetation cover, distance from the ore processing facility, predominant direction of wind, and the longitudinal sequence in relation to a gradient of metal concentrations. At each site, a representative volume per soil samples (0–20 cm depth) was taken from apparently low (S1) to high (S4) pollution levels, and 2 kg sub-sample of sample was taken back to laboratory for sample preparation and analysis. Plant samples were collected from the same sites as the soil samples. At least two to four individuals of all plant species were randomly collected within the sampling areas. Besides the Brassicaceae species Moricandia moricandioides (Boiss.) Heyw. [M. ramburii Webb] that was present at all sites (S1, S2, S3 and S4), two Asteraceae species, Sonchus tenerrimus L. (sites S1, S2 and S3) and Crepis vesicaria L. (site S2), one Plantaginaceae species Plantago amplexicaulis L. (sites S1, S3 and S4) and one Papaveracean species, Glaucium flavum Crantz (site 2) were considered.
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To determine the total soil metal concentrations air dried and sieved samples were ground to a fine powder using an agate ball mill. A subsample of 0.1 g mixed with 2.5 ml of HNO3 and 2.5 ml of water was heated at 90 °C for 3 h in closed vessels. The extract was centrifuged and transferred to a volumetric flask. The residue was transferred to Teflon vessel with 5 ml HF and 2 ml HNO3, keeping it at 90 °C overnight. The extract was transferred to another Teflon vessel with 2 ml HClO4 and the residue was heated again with 5 ml HCl at 90 °C for 2 h. All extracts were transferred to the second Teflon vessel with 2 ml HClO4 and then, evaporated. To the final residue 5 ml of water and 2.5 ml of HNO3 were added and then heated to boil. Finally, it was transferred to the volumetric flask. Metal analysis in the extracts was determined by inductively coupled plasma-mass spectrometer (ICP-MS Perking Elmer Elaw 6000). After immediate transfer to the laboratory plant samples were separated into roots and shoots. The plant material was carefully washed with tap water followed by distilled water. The oven dried (60 °C) plant material was digested in a microwave oven using a mixture (5:1) of HNO3 (65%), H2O2 (30%) in closed vessels. Potentially toxic trace elements in the plant digests were analysed by ICP-ES (Jobin Yvon-VHR 38). Quality control was assured by the use of duplicate analyses performed on all samples, the use of reagent blanks, and a standard reference soil (CRM 141 R, BCR, Brussels), whose analysis yielded Cr, Ni and Cu contents close to the certified values. The average precision was better than 10%. The detection limits for the metals in mg kg − 1 were: Cd (0.1), Cu (0.1), Pb (0.1), Sb (0.07) and Zn (0.8). 2.3. Statistical analysis The data is presented as mean and ±standard deviation. Shoot accumulation factor (SAF) is defined as the ratio of metal concentration in shoots to that in soil which is a measure of the ability of a plant uptake and transport metals to the shoots (Vyslouzilova et al., 2003). The translocation factor (TF) is defined as the ratio of metal concentration in the plant shoot to that in the root (Sun et al., 2008). One way ANOVA was carried out to compare the difference of means from various sampling sites, followed by Bonferroni multiple comparison test (p b 0.05). All statistical evaluations were performed using the SPSS software package (SPSS, 2000). 3. Results and discussion 3.1. Soil properties The physico-chemical properties of the soils of all sampling sites are presented in Table 1. The soils sampled around the galena mine had quite similar physico-chemical properties. At all sampling sites soils had basic pH and no salinity problem according to the values of electrical conductivity. Soils were characterized by high calcium carbonate concentrations, organic matter content between 13 and
2.2. Soil and plant analysis The collected soil samples were transferred to the laboratory, air dried and then sieved through a 2 mm screen. The b 2 mm fraction of the soil samples were stored in paper bags, in dark, dry conditions, at room temperature, for subsequent analysis. The pipette method was used to determine particle size distribution in the soil samples (b2 mm). Soil pH was measured potentiometrically in water at soil-to-solution ratio of 1:2.5 (MAPA, 1994). Organic carbon (OC) content was determined using the Walkley– Black dichromate acid oxidation method. Electrical conductivity (EC) in 1:5 (soil:water) solution was determined by potentiometry and CaCO3 by dissolution with HCl and titration of its excess with NaOH.
Table 1 Selected physico-chemical properties of soils sampled around the Eugenia galena mine in Bellmunt, mean and standard deviation with n = 2 (EC, electrical conductivity; OM, organic matter).
pHw pHKCl EC (dS cm− 1) CaCO3 (g kg− 1) OM (g kg− 1) Sand (%) Silt (%) Clay (%) Texture classes
S1
S2
S3
S4
8.2 ± 0.1 7.3 ± 0.1 0.3 ± 0.1 184 ± 13 24.0 ± 0.3 66.4 ± 2.3 17.2 ± 0.8 16.4 ± 0.3 Sandy loam
7.8 ± 0.2 7.5 ± 0.1 1.2 ± 0.1 277 ± 35 14.0 ± 1.4 79.8 ± 5.4 9.6 ± 4.3 10.5 ± 1.1 Sandy loam
7.8 ± 0.1 7.4 ± 0.1 1.8 ± 0.3 292 ± 18 13.0 ± 1.4 67.8 ± 2.5 21.0 ± 3.4 11.2 ± 0.8 Sandy loam
8.0 ± 0.1 7.6 ± 0.2 1.3 ± 0.2 337 ± 21 14.0 ± 0.9 84.1 ± 2.5 7.7 ± 1.4 8.2 ± 0.5 Loamy sand
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Table 2 Mean total (HF/HNO3 digest) concentrations (mg kg− 1 air dry soil) and standard deviation (n=3) of selected trace elements in soils around the Eugenia galena mine at Bellmunt (Priorat). For any given element, within a row, values followed by the same letter do not differ at p= 0.05.
CuT PbT SbT ZnT
S1
S2
S3
S4
89.3 ± 7.7a 19358 ± 347a 9.7 ± 0.2a 318 ± 5.1a
257 ± 48a 28998 ± 378b 19.5 ± 0.7b 837 ± 96b
387 ± 15.7a 37197 ± 210c 24.5 ± 0.6c 749 ± 4.6b
415 ± 39.4a 38956 ± 356d 31.1 ± 0.6d 989 ± 39.1 b
Table 4 Concentrations and standard deviation of selected trace elements (μg g− 1 dry weight) in shoots (S) and roots (R) of C. vesicaria (n = 4) and G. flavum (n = 2) that only grow at moderate pollution site (S2). Species
Organ
Cu
Pb
Sb
Zn
C. vesicaria
S R S R
15.1 ± 5.3 32.4 ± 21.8 11.2 ± 1.0 60.8 ± 21.7
369 ± 125 1815 ± 265 121 ± 50.3 6968 ± 1187
0.7 ± 0.5 1.1 ± 0.2 0.4 ± 0.0 2.5 ± 0.2
107 ± 30.0 92.6 ± 13.4 114 ± 50.5 379 ± 157
G. flavum
3.3. Plant elemental composition 24 g kg − 1, and a sandy-loam or a loamy sand texture. The local reference topsoil samples (S1) presented the greatest pH (i.e., pH = 8.1) with the smallest calcium carbonate content. 3.2. Soil elemental composition The concentration of heavy metals and metalloids varied greatly (Table 2). Soils from sampling sites S1 and S4 had the smallest and the largest contamination burdens, respectively. All soil samples contained high concentrations of Pb, Zn, Cu and Sb. As expected, the most abundant metal pollutant was Pb, reaching 3.9% in soils of site S4. The total Pb content exceeded the ranges that are considered toxic to normal plants. In soils with a pH greater than 7.0, the established threshold value for agricultural use is 300 mg kg − 1 (BOE, 1990). Similar values were cited by Bernal et al. (2007), and Bowen (1979), while Kabata-Pendias and Mukherjee (2007) and Sheppard et al. (1992) suggested values of 400 mg kg − 1 and 750 mg kg − 1, respectively. The soil metal concentrations found in this study at Bellmunt are higher than those usually reported for superfund sites (Gasser et al., 1996; Pichtel et al., 2001). Zinc was the second most abundant soil contaminant around the mine followed by Cu. However, the concentrations of Zn in Bellmunt mine soils were smaller than those contained in the literature for other sites; e.g. the Monica mine in Spain reported a total Zn concentration of 846 mg kg − 1 or Andacollo mining zone in Northern Chile with 480 mg kg − 1 (Higueras et al., 2004). Soil Sb concentrations were enhanced in relation to local reference topsoil samples (S1), but clearly below the extreme levels reported in the vicinity of smelters (Edwards et al., 1995).
A total of five plant species were investigated for heavy metal concentrations in their tissues as these species were dominating the studied sites (Tables 3 and 4). Metal concentrations in the studied plants were very variable. The greatest shoot Cu, Pb and Sb concentrations were observed in Plantago amplexicaulis (Table 3). However, the greatest Zn shoot concentrations were observed in Moricandia moricandioides. The maximum root metal and Sb concentrations were also found in P. amplexicaulis but always at the most polluted site (S4). It is well-known that another Plantago species, P. lanceolata can adapt to a large diversity of metal-rich habitats because of its potential for fast evolution of tolerance to Zn, As, Cu, and/or Pb (Pollard, 1980). P. lanceolata is widely distributed and has been proposed as a bioindicator for Pb, Zn, and Cd (Dimitrova and Yurukova, 2005). In contrast, P. Amplexicaulis is a therophyte species that is typically found in calcareous maritime soils of the Southern Mediterranean area, in the deserts of Egypt and Israel, and in the Arabian Peninsula (USDA, ARS, 2010). In Spain, P. amplexicaulis is located mainly in the South, in Almeria and Murcia, and can extend up to Castellón (Crespo et al., 2007; de la Torre et al., 1995). In the present study this species was found even further North. Probably the ability to tolerate both draught on the sandy, badly structured soils and high metal content allowed P. amplexicaulis to efficiently compete in the mine soil habitat located in this more Northern region. Glaucium flavum, a species of the Papaveraceae family, typically from calcareous, well-drained marine habitats of the Mediterranean region was only found at site S2 with somewhat lower metal burdens than the other soil with great sand content from site S4. The minimum
Table 3 Concentrations and standard deviation of selected trace elements (μg g− 1 dry weight) in shoots (S) and roots (R) of M. moricandioides (n = 2 at S1, S3 and S4 and n = 4 at S2). P. amplexicaule (n = 2) and S. tenerrimus (n = 2) that only grow at three of the four sampling sites. For any given element, within a row, values followed by the same letter do not differ at p = 0.05. Species
Organ
TE
S1
S2
S3
S4
M. moricandioides
S
Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn Cu Pb Sb Zn
10.3 ± 0.7a 238 ± 19.6a 0.29 ± 0.01a 426 ± 83.7a 11.6 ± 3.0a 1026 ± 569ab 0.66 ± 0.27a 75.7 ± 8.7a 24.3 ± 2.4a 417 ± 37a 1.83 ± 2.21a 257 ± 24a 27.3 ± 5.2a 3996 ± 1071a 1.56 ± 0.10a 155 ± 37a 12.5 ± 5.0a 138 ± 11a 1.21 ± 0.02a 86 ± 1a 29.7 ± 7.4a 4536 ± 659a 3.35 ± 0.69a 128 ± 21a
9.9 ± 2.0a 315 ± 145a 0.52 ± 0.16a 211 ± 19a 12.6 ± 4.4a 1334 ± 511a 1.15 ± 0.23a 59.2 ± 20.0a
6.7 ± 0.1a 550 ± 45a 0.78 ± 0.07a 136 ± 46a 32.3 ± 11.8ab 4417 ± 550bc 3.22 ± 0.30ab 118 ± 9.3ab 39.9 ± 1.4b 7058 ± 293b 3.49 ± 0.16a 314 ± 15a 38.2 ± 13.2a 7705 ± 1175a 3.43 ± 1.19ab 399 ± 19a
27.3 ± 2.3b 1239 ± 263b 1.54 ± 0.34b 879 ± 247b 40.6 ± 9.6b 6209 ± 1815 c 5.33 ± 1.54b 223 ± 56b 19.1 ± 0.3a 1766 ± 85 c 1.25 ± 0.02a 309 ± 16a 119 ± 35.0a 16790 ± 5427a 7.15 ± 1.35b 771 ± 102b 39.5 ± 1.8b 610 ± 134a 1.10 ± 0.46a 312 ± 58a 36.9 ± 1.8a 4005 ± 16a 2.99 ± 0.45a 207 ± 27a
R
P. amplexicaulis
S
R
S. tenerrimus
S
R
34.3 ± 5.1b 620 ± 308a 2.64 ± 0.21b 169 ± 60a 86.0 ± 32.7a 9361 ± 4824a 5.80 ± 1.99a 356 ± 129a
J. Bech et al. / Journal of Geochemical Exploration 113 (2012) 94–99
shoot Pb concentration was observed in G. flavum (Table 4). The most interesting species, however, was M. moricandioides. This Brassicaceae was found at all sampling sites and at all sites the shoot Zn concentrations exceeded those of roots (Table 3). Among all the plant species studied, no one was close to the minimum concentration criteria for considering a hyperaccumulator plant (100 mg kg − 1 in the case of Sb, 1000 mg kg − 1 in the case of Cu and Pb and, 10,000 mg kg − 1 for Zn) (Baker and Brooks, 1989; Brooks, 1998; Cluis, 2004). However, all the investigated plant species collected found to be tolerant to high metal concentrations with excellent adaptation to calcareous soils. 3.4. Phytoaccumulation and translocation in plants Plant's potential for phytoextraction can be estimated by both translocation factor (TF) and shoot accumulation factor (SAF). Plant species exhibiting TF and SAF greater than one are suitable for phytoextraction (Pilon-Smits, 2005). In the present study the SAF values were generally smaller than unity (Fig. 1). Only M. moricandioides had
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Zn shoot accumulation factor greater than one at the reference site (S1). The small SAF values are, in part, due to both the high metal burdens of the mine soils and the fact that here the total and not the pseudototal or extractable soil metal concentration were used for SAF calculation. The TF index revealed clear differences in the root to shoot translocation of Sb and heavy metals (Fig. 2). Among all the plants screened, P. amplexicaulis had highest TF for Cu, Pb and Sb. S. tenerrimus also showed a TF greater than one for Cu in S4. However the most significant results were observed for Zn. Four plant species i.e. M. moricandioides, S. tenerrimus, C. vesicaria and P. amplexicaulis, had a TF greater than one (Fig. 2). M. moricandioides was the only studied plant that showed efficient Zn translocation at all sites (S1, S2, S3 and S4). On all sampling sites, except S3, the shoot Zn concentrations of this species were at least three times higher than those of the roots. At the sampling site with the smallest soil Zn concentration (S1) the TF index for this chemical element even exceeded the value of 5 for M. moricandioides. Reports on high shoot/root metal ratios from field-sampled plant material have to be considered with caution because frequently contamination of the
Fig. 1. Shoot accumulation factor (SAF) of all the plant species collected around the galena mine of Bellmunt.
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Fig. 2. Translocation factor (TF) of all the plant species collected around the galena mine of Bellmunt.
leaves with soil particles cannot be excluded. In the M. moricandioides samples of the present study this was not the case. The soils contained much higher Pb than Zn concentrations. If soil particles would have been present in the shoot samples, a high Pb shoot/root ratio should have been observed. Actually, the Pb shoot/root ratios found in M. moricandioides in any case exceeded the value of 0.2. G. flavum, the species with a great root Pb concentration at site S2, was the most efficient shoot excluder of Pb, exhibiting a shoot to root ratio of only 0.02. Shoot/ root ratios for the other analysed trace elements, Cu, Zn, and Sb, were also small in G. flavum. A possible Zn-accumulation pattern in M. moricandioides was suggested. The great TF values for Zn observed in M. moricandioides are typically found in Zn hyperaccumulating Brassicaceae species such as Thlaspi caerulescens L. (Roosens et al., 2003; Tolrà et al., 1996). However, M. moricandioides should not be considered a Zn-hyperaccumulator as the shoot concentrations did not exceed 900 μg g− 1 dry weight (Table 3), a concentration that is considerably lower than the more than 10,000 μg g− 1 dry weight reported in T. caerulescens (Baker,
1981). This relatively low uptake of Zn could be due to the relatively high pH of the soils which can considerably hamper Zn bioavailability. M. moricandioides has been cited among wild Brassicaceae of interest, because it could be a valuable source of traits related to tolerance to calcareous soils and as a cover crop (Warwick et al., 2009). To our best knowledge this is the first report on possible Zn-accumulating character of M. moricandioides. 4. Conclusions The Bellmunt mining area offers singular conditions for the selection of germplasm that combines tolerance to high metal concentrations, especially Pb and Zn, with excellent adaptation to calcareous soils and draught. These plant species does not meet all the criteria of a hyperaccumulator, but none the less accumulated significant amounts of heavy metals in their tissues. Among the metal resistant plant species able to grow at the Bellmunt mine spoils the most contrasting behaviours were observed in G. flavum and in M. moricandioides. The accumulation
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