Environ Sci Pollut Res DOI 10.1007/s11356-015-4357-2
CONTAMINATION RELATED TO ANTHROPIC ACTIVITIES. CHARACTERIZATION AND REMEDIATION
Mercury transfer from soil to olive trees. A comparison of three different contaminated sites Pablo L. Higueras 1 & José Á. Amorós 2 & José Maria Esbrí 1 & Caridad Pérez-de-los-Reyes 2 & Miguel A. López-Berdonces 1 & Francisco J. García-Navarro 2
Received: 17 December 2014 / Accepted: 10 March 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract Mercury contents in soil and olive tree leaves have been studied in 69 plots around three different source areas of this element in Spain: Almadén (Ciudad Real), Flix (Tarragona) and Jódar (Jaén). Almadén was the world’s largest cinnabar (HgS) mining district and was active until 2003, Flix is the oldest Spanish chlor-alkali plant (CAP) and has been active from 1898 to the present day and Jódar is a decommissioned CAP that was active for 14 years (1977– 1991). Total mercury contents have been measured by highfrequency modulation atomic absorption spectrometry with Zeeman effect (ZAAS-HFM) in the soils and olive tree leaves from the three studied areas. The average soil contents range from 182 μg kg−1 in Flix to 23,488 μg kg−1 in Almadén, while the average leaf content ranges from 161 μg kg−1 in Jódar to 1213 μg kg−1 in Almadén. Despite the wide range of data, a
relationship between soil–leaf contents has been identified: in Almadén and Jódar, multiplicative (bilogarithmic) models show significant correlations (R=0.769 and R=0.484, respectively). Significant correlations were not identified between soil and leaf contents in Flix. The continuous activity of the Flix CAP, which remains open today, can explain the different uptake patterns for mercury, which is mainly atmospheric in origin, in comparison to the other two sites, where activity ceased more than 10 years ago and only soil uptake patterns based on the Michaelis–Menten enzymatic model curve are observed.
Responsible editor: Zhihong Xu
Introduction and background
Pablo L. Higueras has a Ph.D. degree from Universidad de Granada. José A. Amorós has a Ph.D. degree from Universidad Politécnica de Madrid. José Maria Esbrí has a Ph.D. degree from Universidad de Oviedo. Caridad Pérez de los Reyes has a Ph.D. degree from Universidad Politécnica de Madrid. Miguel A. López-Berdonces has a MsS degree from Universidad de Castilla-La Mancha. Francisco J. García-Navarro has a Ph.D. degree from Universidad de Castilla-La Mancha. * Pablo L. Higueras [email protected] 1
Departamento de Ingeniería Geológica y Minera and Instituto de Geología Aplicada, Universidad de Castilla-La Mancha, E.I.M.I. Almadén, 13400 Almadén, Ciudad Real, Spain
2
Escuela de Ingenieros Agrónomos de Ciudad Real and Instituto de Geología Aplicada, Universidad de Castilla-La Mancha, Ronda de Calatrava 7, 13071 Ciudad Real, Spain
Keywords Mercury . Plant uptake . Chlor-alkali . Foliar uptake . Flix . Almadén . Jódar
Mercury (Hg) is a highly toxic element that has detrimental effects on the general population when they consume products that contain certain mercury species (Clarkson and Magos 2006; Carocci et al. 2014 and references therein). The presence of such species in the human trophic chain can be related to the presence in pastures or cultivated soils of mercury species that are transferred to livestock or to vegetables, respectively, as well as to corresponding by-products. Higueras et al. (2012) and Amorós et al. (2013, 2014) studied the transfer of this element from Hg-polluted soils from the Almadén mining district to olive tree and vine leaves. They found notable transfer rates that, in the case of olive trees, did not affect the main food product—olive oil (Higueras et al. 2012). These authors also found evidence for the probable uptake of mercury directly by the leaves, in particular during episodes where high levels of gaseous mercury were present for prolonged periods in the local atmosphere. Numerous authors have suggested
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that atmospheric mercury can be taken up by plants through dry and wet deposition, with these mercury fluxes being bidirectional. However, different plant species can show differences in the uptake patterns (Ericksen et al. 2003; Fay and Gustin 2007; Guédron et al. 2013). The olive tree (Oleae europea L.) is a perennial leaf tree that has been cultivated for centuries mainly around the Mediterranean Basin. In Spain, there are more than 2 million hectares with more than 300 million trees (Barranco et al. 2004). The sites under investigation in this study are located in three of the most important regions for the cultivation of olive trees, namely Andalucía (Jódar), Castilla-La Mancha (Almadén) and Cataluña (Flix). The metabolism of trace elements in plants has been widely studied (Wild 1992; Kabata-Pendias 2001; Marschner 2012). However, each plant–soil system has to be studied individually since the behaviour could differ depending on the elements present in a particular system (Kabata-Pendias 2001; Molina et al. 2006) and on the particular chemical form of the element in the soil. In all previously studied cases, the plant composition (leaves, fruit, juices, tubers, etc.) reflects the chemical properties from the cultivation environment (Bargagli 1995; Kabata-Pendias 2001; Vavoulidou et al. 2004; Molina et al. 2006; Higueras et al. 2012; Amorós et al. 2014). In general terms, structural mineral elements (Bould 1966; Fernández-Escobar et al. 1999) and elements that are difficult for the plant to excrete tend to accumulate with time. This trend has been described previously for Ca (Bould 1966; Fernández-Escobar et al. 1999), Ni (Madejón et al. 2006) and Hg (Higueras et al. 2012; Amorós et al. 2014). In the study described here, we analyzed data for the total mercury contents in soil and olive tree leaves from three different areas, which have different historic avatars regarding this element: (i) the Almadén Hg mining district (on the basis of data published by Higueras et al. (2012), where Hg pollution of soils is a long-lasting and intensively developed process, but metallurgical activity ceased completely in recent times), (ii) the Flix chlor-alkali plant area, which has recently been described as the most important source of atmospheric mercury today (Esbrí et al. 2014), but has caused less significant pollution in local soils, and (iii) the Jódar decommissioned chlor-alkali plant, which was active for 14 years (1977–1991), but was closed and abandoned without any reclamation measures. All of these areas share a Mediterranean climate, with minor variations, and they also have different geographic, geological and population characteristics, which are described below. On these bases, the main aim of this paper was to study the concentration of mercury in soils and olive tree leaves in the aforementioned areas, which are heavily contaminated with mercury, in order to assess the particular behaviour of this element in olive trees under different conditions.
Materials and methods The sites The Almadén mercury mining district Almadén is the most important cinnabar (HgS) mining district worldwide, having produced almost one third of the total industrial production of this element (Hernández et al. 1999). Almadén is located some 300 km SSW of Madrid, in Ciudad Real province, Castilla-La Mancha. The area has a Mediterranean semiarid climate. The area is semi-mountainous, with an altitude between 550 and 1000 m.a.s.l., as conditioned by its geological characteristics, which involve an Appalachian relief with high Sierras produced by quartzitic formations and smooth valleys excavated in shale-dominated formations. These formations correspond to Palaeozoic sequences, which were affected by tectonics and low-grade metamorphism during the Hercynian orogenic event (Hernández et al. 1999 and references therein); these processes condition the physiography of the region. The most important geological feature of this area is the presence of an important number of cinnabar deposits, which have different typologies and different sizes. These deposits include the world’s largest Hg mine (Almadén) and four other smaller mines (Las Cuevas, El Entredicho, Nueva Concepción and Vieja Concepción) with different historic periods of activity. Furthermore, there are up to 60 sites with incipient exploitations or where cinnabar has been cited by different authors, and these sites are scattered in different locations, in different stratigraphic positions and have different degrees of exposure to the surface. All of these differences lead to varied levels of influence on soil contamination and, on this basis, to biota, surface, ground waters, etc. Huckabee et al. (1983), Higueras et al. (2003, 2006), Gray et al. (2004), Moreno et al. (2005), Sánchez et al. (2005), Bernaus et al. (2006), Millán et al. (2006), Molina et al. (2006), Esbrí et al. (2010), Llanos et al. (2010) and Martínez-Coronado et al. (2011), among others, studied the distribution of mercury pollution in soils from the district and also assessed the effects on other environmental compartments. In the years 2006–2008, the mining company carried out a reclamation process on the main mine dump located in the neighbourhood of the urban area; this, together with the cessation of mining and the metallurgic activity in 2003, led to a marked decrease in the concentrations of gaseous mercury in the local atmosphere, as described by Higueras et al. (2013). In this context, the study carried out by Higueras et al. (2012) showed how olive trees grown in the Almadén district have a capacity to accumulate Hg in their leaves. The results of a temporal analysis showed that the Hg uptake during the periods prior to the main dump reclamation was significantly higher than that after this process. This finding was interpreted
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as being a consequence of the capacity of this tree’s leaves to take up gaseous mercury through the stomates. The Flix chlor-alkali plant In the 1890s, Flix was the first important industrial complex in Spain due to a particular feature in the course of the Ebro River, namely a meander that favours the hydroelectric production of electricity. As a consequence, this location was chosen as the site of the first chlor-alkali plant to be built in Spain. This facility is still active and is operated by the chemical company Ercros. The plant is located very close to the town of Flix in the Tarragona province, South Catalonia, Spain. The town has some 4000 inhabitants and includes the old industrial complex, in which some other industries are still in operation besides the chlor-alkali plant, and a rural environment in which olive trees and other fruit trees are cultivated. The climate of the area is coastal Mediterranean with an altitude in the range 40–450 m.a.s.l. From a geological point of view, the area includes mainly Triassic carbonate rocks in the mountains with tertiary clay and shales in the valleys. Esbrí et al. (2014) described the environmental consequences of the activity of this plant in terms of soil and atmospheric pollution by mercury. The study showed how regional Hg pollution is clearly linked to the chlor-alkali plant and that this affects the soils through deposition of atmospheric mercury. The authors also presented a model that was explained by the wind distribution and physiographic characteristics of the area, as confirmed by the Hg contents in local epiphyte lichens. The decommissioned Jódar chlor-alkali plant The Jódar chlor-alkali plant is located in the province of Jaén, in the Andalucia region of SE Spain. The plant is located very close to the Guadalquivir River, the main river in Andalucia, and is approximately equidistant from the localities of Jódar (to the south) and Úbeda (to the north). The local climate is typical Mediterranean with altitudes in the range 350– 1500 m.a.s.l. From a geological point of view, the area corresponds to the Tertiary Guadalquivir basin and is locally characterized by clays, loams, sandstones, dolomites and gypsum. The area is sufficiently far from populated areas but not from the aforementioned river. The plant was active for 14 years (1977 to 1991) and was closed due to suspected adverse effects on the health of plant workers and on the water of the Guadalquivir River. López-Berdonces et al. (2014) described an environmental survey carried out in this area, which included soil geochemistry, olive tree leaf biogeochemistry and local atmospheric Hg concentrations. The area appears to be characterized by low levels of soil mercury contamination,
with low contents also measured in olive tree leaves, and very low concentrations of atmospheric mercury.
Sampling and sample preparation Sampling at the three sites included both soils and olive tree leaves. A similar soil sampling methodology was used for all the sites: removal of the vegetal cover (always sparse in these sites) and excavation with a spade of the first 10–15 cm (topsoil). Samples were stored in plastic bags and sent to the laboratory for preparation and analysis. Olive tree samples were taken from the same locations as the soil samples; the leaves (between 50 and 100) were taken randomly from the three–four olive trees closest to the soil sampling sites. The leaves were stored in paper bags and sent to the laboratory for preparation and analysis. The preparation of both soil and leaf samples involved drying as a first step. The samples were spread out separately, in the open air, for 3–5 days (soils) or 12–15 days (leaves). Soil samples were disaggregated, homogenized and split to obtain two representative subsamples. The first subsample was sieved to a grain size below 2 mm and a 50 g portion was ground in an automatic Agate mortar to a grain size of 100–150 μm and used for metal determinations. The second portion was stored as a bulk sample. Leaves were hand milled and prepared in the same way for the analysis.
Analytical methods Total mercury contents in both soil and leaf samples were obtained by high-frequency modulation atomic absorption spectrometry with Zeeman effect (ZAAS-HFM), using a Lumex RA-915+ device with a pyrolysis attachment (Sholupov et al. 2004). In this procedure, mercury is converted from a bound state to the atomic state by thermal decomposition in a two-section atomizer. The analysis took 1–5 min depending on the metal content. The detection limit for total mercury determinations in soils and plants was 0.5 μg kg−1. Quality control was achieved by analysis of duplicate samples and certified reference materials (CRM: NIST-2710, NIST 2711, BCR 62 and BCR 482).
Statistical procedures Statistical analysis of the data was carried out using the computer program STATGRAPHICS Plus 5.1 (Copyright© 1994– 2000 Statistical Graphics Corp) and Excel 2013 (Copyright© 2014 Microsoft).
Environ Sci Pollut Res Table 1 Average±standard deviation (SD) for Hg contents (μg kg−1) in soil and olive tree leaves in Almadén, Jódar and Flix sites
Site
Average Hg soil content±SD
Average Hg leaf content±SD
Reference
Almadén
Higueras et al. (2012)
23479±37461
1213±1529
Flix
182±106
481±337
Esbrí et al. (2014)a
Jódar
564±889
161±82
See this study (Table 2)
a
Only soil data
Results and discussion Hg in soil and leaves As stated before, Hg content data were obtained from two previous publications specified in Table 1. However, for this study, we added leaf data from Flix (Table 2) and new data, corresponding to both soil and leaf, from Jódar (Table 2). The number of data points (plots controlled) is different for each site: 7 for Almadén, 21 for Flix and 41 for Jódar. As one would expect, the data cover an extremely wide range. The most contaminated soil was found in Almadén close to the dumping zone of the mine (105,000 μg kg−1) and the values are lower for the other two sites (30–40 μg kg−1 in some plots). Mercury content in soil is, as expected, extremely high in the proximity of the mercury mining areas (Almadén and Table 2 Hg contents (μg kg−1) in soil and olive leaves in Jódar and in soil (from Esbrí et al. 2014) and olive leaves in Flix Jódar
Flix
Soil
Olive leaves
Soil
Olive leaves
Soil
Olive leaves
95 95 97 73 92 96 208 138 74 53 422 495
109 119 130 85 46 72 70 223 122 116 176 220
844 447 3825 154 2805 560 1052 1760 1477 254 137 800
91 72 258 120 453 177 367 149 186 188 76 215
84 316 161 172 149 143 90 227 387 371 92 144
333 676 759 715 1220 539 412 1270 676 149 446 565
145 219 199 103 79 245 1605 3215 247
258 103 275 104 112 130 205 176 154
80 138 171 171 30 83 98 254
153 143 147 225 81 225 191 63
129 196 198 377 44 49 98 211 182
488 384 272 216 148 113 144 90 481
Almadenejos) or chlor-alkali plants (Flix and Jódar), and the contents clearly decreased with increasing distance from these pollution sources. Almadén, followed by Jódar, has the highest level of soil contamination, and Flix is the site with the least contaminated soils. World references for Hg contents in soils were reported by Senesi et al. (1999) (mean content in soils 20 μg kg−1) and Kabata-Pendias (2001) (levels of around 90 μg kg−1). It is worth highlighting the marked variations indicated by these two authors even in uncontaminated soils. Higueras et al. (2015) reviewed data for Hg in Spanish soils: the studied data indicate 20 μg kg−1 as a general background level for this element. Such a background value is well below even the lowest concentrations found in the three sites investigated in this work. Leaf Hg contents also range widely, albeit to a lesser extent than for soil, from the most contaminated plot in Almadén (3900 μg kg−1) to the least contaminated plot in Jódar (45 μg kg−1). The sites for Hg leaf contamination in decreasing order are as follows: Almadén>Flix>Jódar. There are very few references in the literature concerning Hg contents in olive trees. Bargagli (1995) determined mercury levels in olive leaves in a background area in Italy and found values in the range 20–180 μg kg−1. In general terms, Kabata-Pendias (2001) reported admissible concentrations for plant tissue (less than 200 μg kg−1) along with toxic concentrations (above 3000 μg kg−1). Despite the high levels detected in the studied sites (some of which were well above the reported toxic concentration), visual evidence of toxic effects was not detected in olive tree leaves (Higueras et al. 2012). Amorós et al. (2014) reported Hg contents in the Almadén
Fig. 1 Hg content (μg kg−1) in soil and olive tree leaves in Jódar, Flix and Almadén sites (logarithmic scale)
Environ Sci Pollut Res Fig. 2 Plot of linear dependence (a; R=0.117, not significant) and multiplicative (bilogarithmic) dependence (b; R=0.269, not significant) between total Hg content (μg kg−1) in soil and olive leaves in Flix
mining district measured in vines (Vitis vinifera, L.), with contents of 5100 μg kg−1 reached, also without visual evidence of toxic symptoms. In a multi-specific wild plant study in the same area, Molina et al. (2006) reported contents from 100 to 106 μg kg−1 depending on the species and the Hg levels in the corresponding soils. It is worth highlighting the relatively high leaf contamination level in Flix, bearing in mind the moderate content in the soil. This finding suggests a different uptake model from that occurring in Almadén and Jódar. Hg relationships in the soil–plant system Mercury concentrations obtained in soil and olive leaves from three different areas under investigation (Almadén, Flix and Jódar) are represented in Fig. 1. Some indications of bilogarithmic correlations between concentrations in leaves and soils are evident from this figure. In order to confirm these correlations, the different possibilities of relationships between the three sets of values were analyzed. Analysis of the data from Flix did not show any kind of relationship between soil and leaf Hg contents. These data are plotted in Fig. 2 on linear and bilogarithmic axes, and the corresponding low R values for these correlation analyses Fig. 3 Plot of statistically significant multiplicative dependence between total Hg content (μg kg−1) in soil and olive leaves in Almadén (a) and Jódar (b)
show that a significant relationship pattern does not exist for either of these possibilities. In the cases of Jódar and Almadén, a relationship was found between Hg contents in soils and leaves from olive trees growing on these soils (Fig. 3). The correlation found is close to the linear model, as suggested in other publications for vines (Amorós et al. 2014) and for olive trees (Higueras et al. 2012), but it fits the multiplicative model better. The pattern is similar to that observed in Michaelis–Menten enzymatic action, cited by many authors (Wild 1992; Marschner 2012) as modelling elemental absorption by plants through the roots. It is worth noting that some of the models for Hg uptake described by Molina et al. (2006) could also be interpreted as being similar to the pattern found in this study. It is also important to note the fact that in these two areas, the level of atmospheric Hg is very low, probably because activity at these sites ceased many years ago (Jódar, where chlor-alkali plant activity ceased in 1991, and Almadén, with mining and metallurgical cessation in 2003 and the main dump reclamation carried out in 2007–2008); on the other hand, the presence of atmospheric Hg in Flix is still very significant (Esbrí et al. 2014). Interpretation of our results indicates that during the activity of the mine, i.e. the metallurgy or the chlor-alkali plant, Hg
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uptake comes from two sources—soil and the atmosphere. The uptake from the soil is influenced by speciation of Hg in this environmental compartment, a factor that is extremely important (Kabata-Pendias 2001; Marschner 2012). Uptake (absorption) from the atmosphere has been described previously for a chlor-alkali plant (CAP) in Grenoble by Guédron et al. (2013) and this is influenced by other factors such as climatology (including wind speed and direction, precipitation, relative humidity, temperature, solar radiation, etc.) and proximity to the emission source. This fact results in a complex scenario, where high Hg concentrations can be found in leaves taken from trees grown on soils with low total Hg contents, as in the case of the Flix area (see Fig. 1). When the presence of gaseous Hg decreases significantly or ceases altogether, the only uptake comes from soils and the process depends on the Hg species present in the soil and these forms need to be bioavailable (Gupta et al. 1996). In Almadén, the main species present in the local soils tends to be cinnabar (Llanos et al. 2011; Esbrí et al. 2010), but the best correlations between leaf Hg concentrations (in vines) and soil concentrations are found when considering the available fraction (Amorós et al. 2014). In the surroundings of CAPs like the Jódar study area, one would probably expect cinnabar to be absent from the local soils since this mineral was not used in the area. However, Biester and Scholz (1997) described speciation data on soils from a CAP in Germany and estimated that mercury appears to have poor availability for plant uptake and that most mercury is in a residual fraction, mainly as Hg0 or binding to organic soil components, although the presence of mercury sulphides could not be confirmed. Furthermore, a study on a chlor-alkali plant in Portugal (Inácio et al. 1998) showed that available mercury in soils surrounding the CAP was less than 3.4 %, which confirms the pattern described in the study by Biester and Scholz (1997) and is quite similar to the scenario in the Almadén mining district. In our study, the apparent slopes of the trends for the sets of data for Almadén and Jódar are quite similar (Fig. 1). This finding demonstrates the need for further studies regarding the detailed characterization of this process when atmospheric uptake is not active. The model for Hg uptake suggests that this element shows similar behaviour to other structural elements (calcium, strontium, manganese, etc.) with similar ionic radii and electrical charge (Bould 1966; Fernández-Escobar et al. 1999; Rollinson 1993; Amorós et al. 2014) that bind with pectins, biothiols and proteins of the cell wall (Kabata-Pendias 2001; Marschner 2012; Carrasco-Gil et al. 2013). These compounds are considered to have the ability to undergo long-distance transport in both root-to-shoot and shoot-to-root directions. Our results suggest that when a CAP (or other source) is active, high atmospheric mercury levels promote foliar uptake and this leads to poor correlation rates between Hgsoil/Hgplant;
when the CAP has been inactive for a long time, root uptake seems to be the predominant process and this leads to better Hgsoil/Hgplant correlation rates.
Conclusions The following conclusions can be derived from the study: & & &
Hg pollution shows different patterns of contamination in olive tree cultures that surround emission points. The patterns depend on the activity of the mine or factory. Active atmospheric Hg sources spread the emissions in the atmosphere and this is an important source of Hg uptake by the olive tree leaves considered in this study. Once the activity ends, the pollution only remains in the soils and the uptake by the plant shows a multiplicative model, which is similar to the Michaelis–Menten enzymatic activity pattern.
Acknowledgments This study has been funded by the Spanish Ministry of Economy and Competitiveness, project CTM2012-33918. Dr. Neil Thompson reviewed the English style.
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Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton, p 413 Llanos W, Higueras P, Oyarzun R, Esbrí JM, López-Berdonces MA, García-Noguero EM, Martínez-Coronado A (2010) The MERS ADE (European Union) project: testing procedures and environmental impact for the safe storage of liquid mercury in the Almadén district, Spain. Sci Total Environ 408(20):4901–4905 Llanos W, Kocman D, Higueras P, Horvat M (2011) Mercury emissions and dispersion models from soils contaminated by cinnabar mining and metallurgy. J Environ Monitor 13(12):3460–3468 López-Berdonces MA, Esbrí JM, Amorós JA, Lorenzo S, FernándezCalderón S, Higueras P, Perez-de-los-Reyes C (2014) Hg contents in soils and olive-tree (Olea europea, L.) leaves from an area affected by elemental mercury pollution (Jódar, SE Spain). Geophysical Research Abstracts (16) EGU2014-7843 http://meetingorganizer. copernicus.org/EGU2014/EGU2014-7843.pdf. Accessed 12 December 2014 Madejón P, Marañón T, Murillo JM (2006) Biomonitoring of trace elements in the leaves and fruits of wild olive and holm oak trees. Sci Total Environ 355:187–203 Marschner P (2012) Marschner’s mineral nutrition of higher plants (3th edition). Elsevier, Germany Martínez-Coronado A, Oyarzun R, Esbrí JM, Llanos W, Higueras P (2011) Sampling high to extremely high Hg concentrations at the Cerco de Almadenejos, Almadén mining district (Spain): the old metallurgical precinct (1794 to 1861 AD) and surrounding areas. J Geochem Explor 109(1–3):70–77 Millán R, Gamarra R, Schmid T, Sierra MJ, Quejido AJ, Sánchez DM, Cardona AI, Fernandez M, Vera R (2006) Mercury content in vegetation and soils of the Almadén mining area (Spain). Sci Total Environ 368(1):79–87 Molina JA, Oyarzun R, Esbrí JM, Higueras P (2006) Mercury accumulation in soils and plants in the Almadén mining district, Spain: one of the most contaminated sites on Earth. Environ Geochem Health 28:487–498 Moreno T, Higueras P, Jones T, McDonald I, Gibbons W (2005) Size fractionation in mercury-bearing airborne particles (HgPM10) at Almadén, Spain: implications for inhalation hazards around old mines. Atmos Environ 39:6409–6419 Rollinson H (1993) Using geochemical data: evaluation, presentation, interpretation. Pearson Ed, Edimburgh. doi: 10.1016/00167037(95)90141-8 Sánchez DM, Quejido AJ, Fernández M, Hernández C, Schmid T, Millán R, González M, Aldea M, Martin R, Morante R (2005) Mercury and trace element fractionation in Almaden soils by application of different sequential extraction procedures. Anal Bioanal Chem 381(8): 1507–1513 Senesi GS, Baldassare G, Senesi N, Radina B (1999) Trace element inputs into soils by anthropogenic activities and implications for human health. Chemosphere 39:343–377 Sholupov S, Pogarev S, Ryzhov V, Mashyanov N, Stroganov A (2004) Zeeman atomic absorption spectrometer RA-915+ for direct determination of mercury in air and complex matrix samples. Fuel Process Technol 85:473–485 Vavoulidou E, Avramides EJ, Papadopoulos P, Dimirkou A (2004) Trace metals in different crop-cultivation systems in Greece. Water Air Soil Pollut 4(2–3):631–640 Wild A (1992) Soil conditions and plant development as Russell. Ed. Mundiprensa, Madrid, 1045 pp. (In Spanish)
CONTAMINATION RELATED TO ANTHROPIC ACTIVITIES. CHARACTERIZATION AND REMEDIATION
Mercury transfer from soil to olive trees. A comparison of three different contaminated sites Pablo L. Higueras 1 & José Á. Amorós 2 & José Maria Esbrí 1 & Caridad Pérez-de-los-Reyes 2 & Miguel A. López-Berdonces 1 & Francisco J. García-Navarro 2
Received: 17 December 2014 / Accepted: 10 March 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract Mercury contents in soil and olive tree leaves have been studied in 69 plots around three different source areas of this element in Spain: Almadén (Ciudad Real), Flix (Tarragona) and Jódar (Jaén). Almadén was the world’s largest cinnabar (HgS) mining district and was active until 2003, Flix is the oldest Spanish chlor-alkali plant (CAP) and has been active from 1898 to the present day and Jódar is a decommissioned CAP that was active for 14 years (1977– 1991). Total mercury contents have been measured by highfrequency modulation atomic absorption spectrometry with Zeeman effect (ZAAS-HFM) in the soils and olive tree leaves from the three studied areas. The average soil contents range from 182 μg kg−1 in Flix to 23,488 μg kg−1 in Almadén, while the average leaf content ranges from 161 μg kg−1 in Jódar to 1213 μg kg−1 in Almadén. Despite the wide range of data, a
relationship between soil–leaf contents has been identified: in Almadén and Jódar, multiplicative (bilogarithmic) models show significant correlations (R=0.769 and R=0.484, respectively). Significant correlations were not identified between soil and leaf contents in Flix. The continuous activity of the Flix CAP, which remains open today, can explain the different uptake patterns for mercury, which is mainly atmospheric in origin, in comparison to the other two sites, where activity ceased more than 10 years ago and only soil uptake patterns based on the Michaelis–Menten enzymatic model curve are observed.
Responsible editor: Zhihong Xu
Introduction and background
Pablo L. Higueras has a Ph.D. degree from Universidad de Granada. José A. Amorós has a Ph.D. degree from Universidad Politécnica de Madrid. José Maria Esbrí has a Ph.D. degree from Universidad de Oviedo. Caridad Pérez de los Reyes has a Ph.D. degree from Universidad Politécnica de Madrid. Miguel A. López-Berdonces has a MsS degree from Universidad de Castilla-La Mancha. Francisco J. García-Navarro has a Ph.D. degree from Universidad de Castilla-La Mancha. * Pablo L. Higueras [email protected] 1
Departamento de Ingeniería Geológica y Minera and Instituto de Geología Aplicada, Universidad de Castilla-La Mancha, E.I.M.I. Almadén, 13400 Almadén, Ciudad Real, Spain
2
Escuela de Ingenieros Agrónomos de Ciudad Real and Instituto de Geología Aplicada, Universidad de Castilla-La Mancha, Ronda de Calatrava 7, 13071 Ciudad Real, Spain
Keywords Mercury . Plant uptake . Chlor-alkali . Foliar uptake . Flix . Almadén . Jódar
Mercury (Hg) is a highly toxic element that has detrimental effects on the general population when they consume products that contain certain mercury species (Clarkson and Magos 2006; Carocci et al. 2014 and references therein). The presence of such species in the human trophic chain can be related to the presence in pastures or cultivated soils of mercury species that are transferred to livestock or to vegetables, respectively, as well as to corresponding by-products. Higueras et al. (2012) and Amorós et al. (2013, 2014) studied the transfer of this element from Hg-polluted soils from the Almadén mining district to olive tree and vine leaves. They found notable transfer rates that, in the case of olive trees, did not affect the main food product—olive oil (Higueras et al. 2012). These authors also found evidence for the probable uptake of mercury directly by the leaves, in particular during episodes where high levels of gaseous mercury were present for prolonged periods in the local atmosphere. Numerous authors have suggested
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that atmospheric mercury can be taken up by plants through dry and wet deposition, with these mercury fluxes being bidirectional. However, different plant species can show differences in the uptake patterns (Ericksen et al. 2003; Fay and Gustin 2007; Guédron et al. 2013). The olive tree (Oleae europea L.) is a perennial leaf tree that has been cultivated for centuries mainly around the Mediterranean Basin. In Spain, there are more than 2 million hectares with more than 300 million trees (Barranco et al. 2004). The sites under investigation in this study are located in three of the most important regions for the cultivation of olive trees, namely Andalucía (Jódar), Castilla-La Mancha (Almadén) and Cataluña (Flix). The metabolism of trace elements in plants has been widely studied (Wild 1992; Kabata-Pendias 2001; Marschner 2012). However, each plant–soil system has to be studied individually since the behaviour could differ depending on the elements present in a particular system (Kabata-Pendias 2001; Molina et al. 2006) and on the particular chemical form of the element in the soil. In all previously studied cases, the plant composition (leaves, fruit, juices, tubers, etc.) reflects the chemical properties from the cultivation environment (Bargagli 1995; Kabata-Pendias 2001; Vavoulidou et al. 2004; Molina et al. 2006; Higueras et al. 2012; Amorós et al. 2014). In general terms, structural mineral elements (Bould 1966; Fernández-Escobar et al. 1999) and elements that are difficult for the plant to excrete tend to accumulate with time. This trend has been described previously for Ca (Bould 1966; Fernández-Escobar et al. 1999), Ni (Madejón et al. 2006) and Hg (Higueras et al. 2012; Amorós et al. 2014). In the study described here, we analyzed data for the total mercury contents in soil and olive tree leaves from three different areas, which have different historic avatars regarding this element: (i) the Almadén Hg mining district (on the basis of data published by Higueras et al. (2012), where Hg pollution of soils is a long-lasting and intensively developed process, but metallurgical activity ceased completely in recent times), (ii) the Flix chlor-alkali plant area, which has recently been described as the most important source of atmospheric mercury today (Esbrí et al. 2014), but has caused less significant pollution in local soils, and (iii) the Jódar decommissioned chlor-alkali plant, which was active for 14 years (1977–1991), but was closed and abandoned without any reclamation measures. All of these areas share a Mediterranean climate, with minor variations, and they also have different geographic, geological and population characteristics, which are described below. On these bases, the main aim of this paper was to study the concentration of mercury in soils and olive tree leaves in the aforementioned areas, which are heavily contaminated with mercury, in order to assess the particular behaviour of this element in olive trees under different conditions.
Materials and methods The sites The Almadén mercury mining district Almadén is the most important cinnabar (HgS) mining district worldwide, having produced almost one third of the total industrial production of this element (Hernández et al. 1999). Almadén is located some 300 km SSW of Madrid, in Ciudad Real province, Castilla-La Mancha. The area has a Mediterranean semiarid climate. The area is semi-mountainous, with an altitude between 550 and 1000 m.a.s.l., as conditioned by its geological characteristics, which involve an Appalachian relief with high Sierras produced by quartzitic formations and smooth valleys excavated in shale-dominated formations. These formations correspond to Palaeozoic sequences, which were affected by tectonics and low-grade metamorphism during the Hercynian orogenic event (Hernández et al. 1999 and references therein); these processes condition the physiography of the region. The most important geological feature of this area is the presence of an important number of cinnabar deposits, which have different typologies and different sizes. These deposits include the world’s largest Hg mine (Almadén) and four other smaller mines (Las Cuevas, El Entredicho, Nueva Concepción and Vieja Concepción) with different historic periods of activity. Furthermore, there are up to 60 sites with incipient exploitations or where cinnabar has been cited by different authors, and these sites are scattered in different locations, in different stratigraphic positions and have different degrees of exposure to the surface. All of these differences lead to varied levels of influence on soil contamination and, on this basis, to biota, surface, ground waters, etc. Huckabee et al. (1983), Higueras et al. (2003, 2006), Gray et al. (2004), Moreno et al. (2005), Sánchez et al. (2005), Bernaus et al. (2006), Millán et al. (2006), Molina et al. (2006), Esbrí et al. (2010), Llanos et al. (2010) and Martínez-Coronado et al. (2011), among others, studied the distribution of mercury pollution in soils from the district and also assessed the effects on other environmental compartments. In the years 2006–2008, the mining company carried out a reclamation process on the main mine dump located in the neighbourhood of the urban area; this, together with the cessation of mining and the metallurgic activity in 2003, led to a marked decrease in the concentrations of gaseous mercury in the local atmosphere, as described by Higueras et al. (2013). In this context, the study carried out by Higueras et al. (2012) showed how olive trees grown in the Almadén district have a capacity to accumulate Hg in their leaves. The results of a temporal analysis showed that the Hg uptake during the periods prior to the main dump reclamation was significantly higher than that after this process. This finding was interpreted
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as being a consequence of the capacity of this tree’s leaves to take up gaseous mercury through the stomates. The Flix chlor-alkali plant In the 1890s, Flix was the first important industrial complex in Spain due to a particular feature in the course of the Ebro River, namely a meander that favours the hydroelectric production of electricity. As a consequence, this location was chosen as the site of the first chlor-alkali plant to be built in Spain. This facility is still active and is operated by the chemical company Ercros. The plant is located very close to the town of Flix in the Tarragona province, South Catalonia, Spain. The town has some 4000 inhabitants and includes the old industrial complex, in which some other industries are still in operation besides the chlor-alkali plant, and a rural environment in which olive trees and other fruit trees are cultivated. The climate of the area is coastal Mediterranean with an altitude in the range 40–450 m.a.s.l. From a geological point of view, the area includes mainly Triassic carbonate rocks in the mountains with tertiary clay and shales in the valleys. Esbrí et al. (2014) described the environmental consequences of the activity of this plant in terms of soil and atmospheric pollution by mercury. The study showed how regional Hg pollution is clearly linked to the chlor-alkali plant and that this affects the soils through deposition of atmospheric mercury. The authors also presented a model that was explained by the wind distribution and physiographic characteristics of the area, as confirmed by the Hg contents in local epiphyte lichens. The decommissioned Jódar chlor-alkali plant The Jódar chlor-alkali plant is located in the province of Jaén, in the Andalucia region of SE Spain. The plant is located very close to the Guadalquivir River, the main river in Andalucia, and is approximately equidistant from the localities of Jódar (to the south) and Úbeda (to the north). The local climate is typical Mediterranean with altitudes in the range 350– 1500 m.a.s.l. From a geological point of view, the area corresponds to the Tertiary Guadalquivir basin and is locally characterized by clays, loams, sandstones, dolomites and gypsum. The area is sufficiently far from populated areas but not from the aforementioned river. The plant was active for 14 years (1977 to 1991) and was closed due to suspected adverse effects on the health of plant workers and on the water of the Guadalquivir River. López-Berdonces et al. (2014) described an environmental survey carried out in this area, which included soil geochemistry, olive tree leaf biogeochemistry and local atmospheric Hg concentrations. The area appears to be characterized by low levels of soil mercury contamination,
with low contents also measured in olive tree leaves, and very low concentrations of atmospheric mercury.
Sampling and sample preparation Sampling at the three sites included both soils and olive tree leaves. A similar soil sampling methodology was used for all the sites: removal of the vegetal cover (always sparse in these sites) and excavation with a spade of the first 10–15 cm (topsoil). Samples were stored in plastic bags and sent to the laboratory for preparation and analysis. Olive tree samples were taken from the same locations as the soil samples; the leaves (between 50 and 100) were taken randomly from the three–four olive trees closest to the soil sampling sites. The leaves were stored in paper bags and sent to the laboratory for preparation and analysis. The preparation of both soil and leaf samples involved drying as a first step. The samples were spread out separately, in the open air, for 3–5 days (soils) or 12–15 days (leaves). Soil samples were disaggregated, homogenized and split to obtain two representative subsamples. The first subsample was sieved to a grain size below 2 mm and a 50 g portion was ground in an automatic Agate mortar to a grain size of 100–150 μm and used for metal determinations. The second portion was stored as a bulk sample. Leaves were hand milled and prepared in the same way for the analysis.
Analytical methods Total mercury contents in both soil and leaf samples were obtained by high-frequency modulation atomic absorption spectrometry with Zeeman effect (ZAAS-HFM), using a Lumex RA-915+ device with a pyrolysis attachment (Sholupov et al. 2004). In this procedure, mercury is converted from a bound state to the atomic state by thermal decomposition in a two-section atomizer. The analysis took 1–5 min depending on the metal content. The detection limit for total mercury determinations in soils and plants was 0.5 μg kg−1. Quality control was achieved by analysis of duplicate samples and certified reference materials (CRM: NIST-2710, NIST 2711, BCR 62 and BCR 482).
Statistical procedures Statistical analysis of the data was carried out using the computer program STATGRAPHICS Plus 5.1 (Copyright© 1994– 2000 Statistical Graphics Corp) and Excel 2013 (Copyright© 2014 Microsoft).
Environ Sci Pollut Res Table 1 Average±standard deviation (SD) for Hg contents (μg kg−1) in soil and olive tree leaves in Almadén, Jódar and Flix sites
Site
Average Hg soil content±SD
Average Hg leaf content±SD
Reference
Almadén
Higueras et al. (2012)
23479±37461
1213±1529
Flix
182±106
481±337
Esbrí et al. (2014)a
Jódar
564±889
161±82
See this study (Table 2)
a
Only soil data
Results and discussion Hg in soil and leaves As stated before, Hg content data were obtained from two previous publications specified in Table 1. However, for this study, we added leaf data from Flix (Table 2) and new data, corresponding to both soil and leaf, from Jódar (Table 2). The number of data points (plots controlled) is different for each site: 7 for Almadén, 21 for Flix and 41 for Jódar. As one would expect, the data cover an extremely wide range. The most contaminated soil was found in Almadén close to the dumping zone of the mine (105,000 μg kg−1) and the values are lower for the other two sites (30–40 μg kg−1 in some plots). Mercury content in soil is, as expected, extremely high in the proximity of the mercury mining areas (Almadén and Table 2 Hg contents (μg kg−1) in soil and olive leaves in Jódar and in soil (from Esbrí et al. 2014) and olive leaves in Flix Jódar
Flix
Soil
Olive leaves
Soil
Olive leaves
Soil
Olive leaves
95 95 97 73 92 96 208 138 74 53 422 495
109 119 130 85 46 72 70 223 122 116 176 220
844 447 3825 154 2805 560 1052 1760 1477 254 137 800
91 72 258 120 453 177 367 149 186 188 76 215
84 316 161 172 149 143 90 227 387 371 92 144
333 676 759 715 1220 539 412 1270 676 149 446 565
145 219 199 103 79 245 1605 3215 247
258 103 275 104 112 130 205 176 154
80 138 171 171 30 83 98 254
153 143 147 225 81 225 191 63
129 196 198 377 44 49 98 211 182
488 384 272 216 148 113 144 90 481
Almadenejos) or chlor-alkali plants (Flix and Jódar), and the contents clearly decreased with increasing distance from these pollution sources. Almadén, followed by Jódar, has the highest level of soil contamination, and Flix is the site with the least contaminated soils. World references for Hg contents in soils were reported by Senesi et al. (1999) (mean content in soils 20 μg kg−1) and Kabata-Pendias (2001) (levels of around 90 μg kg−1). It is worth highlighting the marked variations indicated by these two authors even in uncontaminated soils. Higueras et al. (2015) reviewed data for Hg in Spanish soils: the studied data indicate 20 μg kg−1 as a general background level for this element. Such a background value is well below even the lowest concentrations found in the three sites investigated in this work. Leaf Hg contents also range widely, albeit to a lesser extent than for soil, from the most contaminated plot in Almadén (3900 μg kg−1) to the least contaminated plot in Jódar (45 μg kg−1). The sites for Hg leaf contamination in decreasing order are as follows: Almadén>Flix>Jódar. There are very few references in the literature concerning Hg contents in olive trees. Bargagli (1995) determined mercury levels in olive leaves in a background area in Italy and found values in the range 20–180 μg kg−1. In general terms, Kabata-Pendias (2001) reported admissible concentrations for plant tissue (less than 200 μg kg−1) along with toxic concentrations (above 3000 μg kg−1). Despite the high levels detected in the studied sites (some of which were well above the reported toxic concentration), visual evidence of toxic effects was not detected in olive tree leaves (Higueras et al. 2012). Amorós et al. (2014) reported Hg contents in the Almadén
Fig. 1 Hg content (μg kg−1) in soil and olive tree leaves in Jódar, Flix and Almadén sites (logarithmic scale)
Environ Sci Pollut Res Fig. 2 Plot of linear dependence (a; R=0.117, not significant) and multiplicative (bilogarithmic) dependence (b; R=0.269, not significant) between total Hg content (μg kg−1) in soil and olive leaves in Flix
mining district measured in vines (Vitis vinifera, L.), with contents of 5100 μg kg−1 reached, also without visual evidence of toxic symptoms. In a multi-specific wild plant study in the same area, Molina et al. (2006) reported contents from 100 to 106 μg kg−1 depending on the species and the Hg levels in the corresponding soils. It is worth highlighting the relatively high leaf contamination level in Flix, bearing in mind the moderate content in the soil. This finding suggests a different uptake model from that occurring in Almadén and Jódar. Hg relationships in the soil–plant system Mercury concentrations obtained in soil and olive leaves from three different areas under investigation (Almadén, Flix and Jódar) are represented in Fig. 1. Some indications of bilogarithmic correlations between concentrations in leaves and soils are evident from this figure. In order to confirm these correlations, the different possibilities of relationships between the three sets of values were analyzed. Analysis of the data from Flix did not show any kind of relationship between soil and leaf Hg contents. These data are plotted in Fig. 2 on linear and bilogarithmic axes, and the corresponding low R values for these correlation analyses Fig. 3 Plot of statistically significant multiplicative dependence between total Hg content (μg kg−1) in soil and olive leaves in Almadén (a) and Jódar (b)
show that a significant relationship pattern does not exist for either of these possibilities. In the cases of Jódar and Almadén, a relationship was found between Hg contents in soils and leaves from olive trees growing on these soils (Fig. 3). The correlation found is close to the linear model, as suggested in other publications for vines (Amorós et al. 2014) and for olive trees (Higueras et al. 2012), but it fits the multiplicative model better. The pattern is similar to that observed in Michaelis–Menten enzymatic action, cited by many authors (Wild 1992; Marschner 2012) as modelling elemental absorption by plants through the roots. It is worth noting that some of the models for Hg uptake described by Molina et al. (2006) could also be interpreted as being similar to the pattern found in this study. It is also important to note the fact that in these two areas, the level of atmospheric Hg is very low, probably because activity at these sites ceased many years ago (Jódar, where chlor-alkali plant activity ceased in 1991, and Almadén, with mining and metallurgical cessation in 2003 and the main dump reclamation carried out in 2007–2008); on the other hand, the presence of atmospheric Hg in Flix is still very significant (Esbrí et al. 2014). Interpretation of our results indicates that during the activity of the mine, i.e. the metallurgy or the chlor-alkali plant, Hg
Environ Sci Pollut Res
uptake comes from two sources—soil and the atmosphere. The uptake from the soil is influenced by speciation of Hg in this environmental compartment, a factor that is extremely important (Kabata-Pendias 2001; Marschner 2012). Uptake (absorption) from the atmosphere has been described previously for a chlor-alkali plant (CAP) in Grenoble by Guédron et al. (2013) and this is influenced by other factors such as climatology (including wind speed and direction, precipitation, relative humidity, temperature, solar radiation, etc.) and proximity to the emission source. This fact results in a complex scenario, where high Hg concentrations can be found in leaves taken from trees grown on soils with low total Hg contents, as in the case of the Flix area (see Fig. 1). When the presence of gaseous Hg decreases significantly or ceases altogether, the only uptake comes from soils and the process depends on the Hg species present in the soil and these forms need to be bioavailable (Gupta et al. 1996). In Almadén, the main species present in the local soils tends to be cinnabar (Llanos et al. 2011; Esbrí et al. 2010), but the best correlations between leaf Hg concentrations (in vines) and soil concentrations are found when considering the available fraction (Amorós et al. 2014). In the surroundings of CAPs like the Jódar study area, one would probably expect cinnabar to be absent from the local soils since this mineral was not used in the area. However, Biester and Scholz (1997) described speciation data on soils from a CAP in Germany and estimated that mercury appears to have poor availability for plant uptake and that most mercury is in a residual fraction, mainly as Hg0 or binding to organic soil components, although the presence of mercury sulphides could not be confirmed. Furthermore, a study on a chlor-alkali plant in Portugal (Inácio et al. 1998) showed that available mercury in soils surrounding the CAP was less than 3.4 %, which confirms the pattern described in the study by Biester and Scholz (1997) and is quite similar to the scenario in the Almadén mining district. In our study, the apparent slopes of the trends for the sets of data for Almadén and Jódar are quite similar (Fig. 1). This finding demonstrates the need for further studies regarding the detailed characterization of this process when atmospheric uptake is not active. The model for Hg uptake suggests that this element shows similar behaviour to other structural elements (calcium, strontium, manganese, etc.) with similar ionic radii and electrical charge (Bould 1966; Fernández-Escobar et al. 1999; Rollinson 1993; Amorós et al. 2014) that bind with pectins, biothiols and proteins of the cell wall (Kabata-Pendias 2001; Marschner 2012; Carrasco-Gil et al. 2013). These compounds are considered to have the ability to undergo long-distance transport in both root-to-shoot and shoot-to-root directions. Our results suggest that when a CAP (or other source) is active, high atmospheric mercury levels promote foliar uptake and this leads to poor correlation rates between Hgsoil/Hgplant;
when the CAP has been inactive for a long time, root uptake seems to be the predominant process and this leads to better Hgsoil/Hgplant correlation rates.
Conclusions The following conclusions can be derived from the study: & & &
Hg pollution shows different patterns of contamination in olive tree cultures that surround emission points. The patterns depend on the activity of the mine or factory. Active atmospheric Hg sources spread the emissions in the atmosphere and this is an important source of Hg uptake by the olive tree leaves considered in this study. Once the activity ends, the pollution only remains in the soils and the uptake by the plant shows a multiplicative model, which is similar to the Michaelis–Menten enzymatic activity pattern.
Acknowledgments This study has been funded by the Spanish Ministry of Economy and Competitiveness, project CTM2012-33918. Dr. Neil Thompson reviewed the English style.
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