SOILS, SEC 1 • SOIL ORGANIC MATTER DYNAMICS AND NUTRIENT CYCLING • RESEARCH ARTICLE

Aluminium geochemistry in the bulk and rhizosphericsoil of the species colonising an abandoned copper minein Galicia (NW Spain)

Esperanza Álvarez & María Fernández-Sanjurjo &

Xosé Luis Otero & Felipe Macías

Received: 28 October 2009 /Accepted: 25 April 2010 /Published online: 21 May 2010# Springer-Verlag 2010

AbstractPurpose Aluminium partitioning in the solid fraction andaluminium in solution in the bulk and rhizospheric soil ofdifferent plant species colonising an abandoned Cu mineslope (Calluna vulgaris, Erica cinerea and Salix atroci-nerea) and mine dump (C. vulgaris and E. cinerea) wereinvestigated. The aim of the study was to determine thechanges that the species induce in the Al forms in therhizosphere in order to adapt to heterogeneous substrates.Materials and methods Al was extracted from the solidphase with different solutions: ammonium oxalate (Alo),sodium pyrophosphate (Alp), copper chloride (Alcu),lanthanum chloride (Alla) and ammonium chloride(AlNH4). The following Al fractions were obtained:inorganic non-crystalline Al (Alop=Alo–Alp), highly stableorganoaluminium complexes (Alpcu=Alp-Alcu), organo-aluminium complexes of intermediate stability (Alcula=Alcu–Alla) and labile organoaluminium complexes (Alla).The concentration of Al present in the aqueous phase wasalso determined.Results and discussion The pH of the soil in the mine slopewas close to 7, and the roots of Ericaceae caused strongacidification so that the pH of the rhizospheric soil was low(3.6–4.7). In contrast, the pH of the bulk and the rhizo-

spheric soil of S. atrocinerea remained close to 7. In themine dump (pH3.7), the changes in the pH of the Ericaceaerhizosphere in relation to the bulk soil were not as markedas in the mine slope. Alop predominated in the solid phase(more than 70% of the Alo), and Alpcu predominated in theorganoaluminium complexes (more than 55%), followed byAlcula (13% and 47%) and Alla (3% and 21%). Theconcentration of Al in solution was significantly related tothe concentrations of AlNH4 (r=0.43), Alla (r=0.50) andAlcula (r=0.45).Conclusions Ericaceae species grew in dump and slopematerials because they modified the pH of the rhizosphericsoil, while S. atrocinerea only grew in areas where the soilconditions were close to neutral. The concentration ofaluminium fractions was higher in the Ericaceae rhizo-sphere soil than in Ericaceae bulk soil, S. atrocinerearhizosphere and bulk soils. Moreover, highly stable organo-aluminium complexes predominated, and the dissolved Alconcentration was low, despite the strong acidity.

Keywords Al partitioning .Calluna vulgaris .Ericacinerea . Mine soils . Rhizospheric Al . Salix atrocinerea

1 Introduction

The largest geological area of copper mineralization inGalicia (NW Spain) is associated with the Precambrianbasic massif near Santiago de Compostela and consistsalmost totally of amphibolic-type rocks. The Touro depositconsists of mineralized Fe and Cu sulphides (pyrite,pyrrhotite, chalcopyrite etc.), which occur in variableconcentrations in the mine spoils. Weathering of theseminerals initiates highly complex oxidation processesincluding redox, hydrolysis, complexation and solution–

Responsible editor: Chris Johnson

E. Álvarez (*) :M. Fernández-Sanjurjo :X. L. OteroEscuela Politécnica Superior, Depto. Edafología y QuímicaAgrícola, Universidad de Santiago de Compostela,Campus Universtario,27002 Lugo, Spaine-mail: esperanza.alvarez@usc.es

F. MacíasFacultad de Biología, Dpto. Edafología y Química Agrícola,Universidad de Santiago de Compostela, Campus sur,15782 Santiago de Compostela, Spain

J Soils Sediments (2010) 10:1236–1245DOI 10.1007/s11368-010-0245-z

precipitation reactions, resulting in a large release ofprotons and mobilisation of toxic elements such asaluminium and trace elements (Álvarez et al. 1993;Alvarez-Valero et al. 2009; Lizarraga-Mendiola et al.2009). Revegetation is one of the most effective methodsof achieving sustainable site restoration and visual im-provement of land degraded by mining (Remon et al.2005). However, the soil in the derelict land remaining aftermetal mining is usually unfavourable for plant growth andincludes high levels of toxic metals (Rotkittikhun et al.2006) and extreme pH (Conesa et al. 2006).

Most plants become stressed in acid soils as result oftoxic concentrations of Al (Foy 1984). However, manyplant species are naturally adapted to such conditions andcan grow in very acidic soils without suffering any damage.It is generally agreed that the toxicity of Al is low when themetal is complexed with organic ligands (Kinraide 1997;Kinraide et al. 2005); this may partly explain the apparentlack of any deleterious effect of Al on the growth of plantspecies in acid soils. Moreover, plants adapted to such soilshave developed strategies for tolerating acid conditions(Marschner 1991). These strategies, which include root-induced modifications of the rhizosphere, such as changesin the cation–anion uptake ratio (Haynes 1990), as well asexudation of Al chelators (Jones 1998; Ma and Furukawa2003), may affect the distribution of Al within the differentsolid fractions and may play an important role in degradingthe soil (Barceló and Poschenrieder 2002; Ma andFurukawa 2003). However, some authors (Göttlein et al.1999; Camps et al. 2003) have found higher concentrationsof Al3+, which was probably released when root-exudedprotons were buffered by the soil. The rhizosphere is adynamic microenvironment, in which many new substancesare constantly released and in which more secondarycompounds will be produced under environmental stress(López-Bucio et al. 2000).

Numerous studies have been carried out in hyperacidenvironments similar to that considered in the present study,and several have been undertaken to determine the impactof drainage waters on nearby rivers and estuaries; however,most of these studies have focused on the mobilisation andfractionation of heavy metals in soils and waters (Morrilloet al. 2002; Galán et al. 2003; Sánchez-España et al. 2005;Nieto et al. 2007; Pérez-López et al. 2007). However,studies involving the geochemistry of Al in mine soils arescarce (see e.g. Monterroso et al. 1994, 1998), while as faras we know, there are no studies of Al fractionation in therhizospheric soil for this type of substrate. However, it iswidely recognised that plants alter the chemistry of soilsolutions around their roots. Previous studies have shownthat the pH of the rhizosphere soil solution is lower (as lowas 3) than that of the surrounding soil solution (pH5–7;Arthur and Fahey 1993; Marschner and Romheld 1983).

Such differences in pH have important implications asregards the geochemical behaviour of aluminium. In aprevious study carried out in the same zone, the forms of Alpresent in surface water and soil solution were identified,and it was found that in heavily contaminated zones, mostof the Al is present as the labile forms Al-SO4 and Al3+

species, whereas in non-contaminated rivers, fluoride-bound forms predominate. In the former, Al activity in thewater and soil solution appears to be controlled by jurbaniteor alunite type minerals and in non-contaminated rivers bygibbsite and phyllosilicate type minerals (Álvarez et al.1993).

The main objective of the present study was toinvestigate the Al forms present in the solid fraction andthe Al in solution. Unlike in previous studies, the soilsamples were separated into bulk, external and internalrhizosphere soil of different species growing spontaneouslyon the Touro Cu mine slope (Calluna vulgaris, Ericacinerea and Salix atrocinerea) and on the mine dump (C.vulgaris and E. cinerea). The results of the study mayprovide useful information about the conditions underwhich certain plants colonise marginal environments suchas mine soils.

2 Materials and methods

The study was carried out at the Touro copper mine (NWSpain; Fig. 1), which operated until the 1980s. Thegeological substrate is amphibolite. The mine dumpconsists of spoils resulting from mining activities andcontains large amounts of sulphides such as pyrite,pyrrhotite and chalcopyrite.

The spoil dump, mine slope and other surfaces of thequarry have conserved a variable content of metalsulphides, oxidation of which may produce strong acidifi-cation of the soil (Calvo de Anta et al. 1991; Calvo andPérez 1993). These deposits were exploited in an open castmine, which occupies an area of 390 ha, and at present, themine slopes and dumps are in the process of being restored(see Fig. 1). The main characteristics of the mine slope anddump are shown in Table 1. The concentration of P in thewaste is low (as measured by the Olsen method: Olsen andSommers 1982), and concentrations of exchangeable Caand Al differ in the mine slope and mine dump. Theconcentrations of available heavy metals (as measured bythe Mehlich method: Mehlich 1984) were not phytotoxic,expect for those of Cu (>56 mg kg−1, Monterroso et al.1998).

The samples of bulk and rizospheric soil were collectedin November 2005, from the Touro mine slope andassociated dump. After initial characterization of the area(Jorge 2007), two small homogeneous sites in the mine

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dump (∼1.5 ha) and mine slope (∼1.3 ha) were selected forstudy. However, vegetation only grew spontaneously in onearea that represents approximately 10% of the surface areaof the zones under study. In the revegetated zone of thestudy areas (slope and dump mine), three plots (surface area20 m2) were established for sample collection. The bulksoil was considered the same for all species in a plot,because of the homogeneity of the area (Jorge 2007). Fivesamples of bulk soil were collected in each plot and mixedto provide a composite sample. The bulk samples werecollected from around the plants, at a distance of approx-imately 50 cm; this was possible because of the low densityof vegetation.

The rhizospheric soil samples were collected in tripli-cate, from plant species growing spontaneously in the zone(C. vulgaris, S. atrocinerea and E. cinerea), by the methoddescribed by Chung and Zazoski (1994). The roots wereseparated from the soil and gently shaken. The particlesdetached during shaking were combined to provide afraction designated external rhizosphere (ER). The particlesremaining attached to the roots were removed by vigorousshaking and by brushing with a toothbrush; this fractionwas designated the internal rhizosphere (IR).

Once the bulk soil and the internal and externalrhizosphere soil were separated, the samples were dried at40°C and sieved through a 2-mm sieve. The followingdeterminations were performed in the soil solid fraction: pHin water and in 0.1 M KCl (Guitián and Carballas 1976);the total C, N and S with a LECO CNS-2000 autoanalyzer;effective cation exchange capacity (eCEC), as the sum ofCa, Mg, Na, K and Al (Kamprath 1970) displaced by 1 MNH4Cl (Peech et al. 1947) and determined by atomicabsorption (Ca, Mg and Al) and atomic emission (Na andK) spectrophotometry and Al saturation. Different forms ofaluminium were extracted from the soil solid fraction bynon-sequential extraction with different reagents. Total Alwas extracted by adding a mixture of HNO3/HF (3:5 v/v) ina 120-ml Teflon bomb containing 0.5 g of ground soilsample and heating the mixture in an Ethos Plus microwavelab station for 30 min (the efficiency of the extractionprocess was >90%; see Otero et al. 2005). The otherfractions were extracted with acid oxalate (ratio soil:extractant 1:100, with 4 h shaking), sodium pyrophosphate(ratio soil:extractant 1:100, with 16 h shaking), 0.5 MCuCl2 (ratio soil: extractant 1:10, 30 min shaking, repose12 h), LaCl3 (ratio soil:extractant 1:10, with 2 h shaking)and unbuffered NH4Cl (ratio soil:extractant 1:20, contacttime, 12 h). Aluminium in the extracts was determined by

Fig. 1 Location of the studyarea and sampling points

Table 1 Characteristics of the material present in the Touro mineslope and dump

Mine slope Mine dump

Electrical conductivity (dS m−1) 0.29 0.08

SO4−2 (mg kg−1) 94.03 27.10

Olsen P (mg kg−1) 0.79 0.89

Exchangeable Ca (cmol(+)kg−1) 16.28 0.28

Exchangeable Mg (cmol(+)kg−1) 0.56 0.25

Exchangeable Na (cmol(+)kg−1) 0.07 0.04

Exchangeable K (cmol(+)kg−1) 0.05 0.04

Exchangeable Al (cmol(+)kg−1) 0.34 2.16

Effective CEC (cmol(+)kg−1) 17.30 2.76

Total Al (mg kg−1) 14.200 13.765

Available Fe (mg kg−1) 417.75 315.88

Available Mn (mg kg−1) 46.31 1.62

Available Cu (mg kg−1) 90.42 55.81

Available Zn (mg kg−1) 7.10 1.79

Available Pb (mg kg−1) 0.23 0.53

Available Ni (mg kg−1) 4.13 0.40

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atomic absorption spectrophotometry (Varian, SpectrAA-220FS). Reference materials were used to ensure thereliability of the results. The limit of detection of Al byatomic adsorption spectrophotometry was 0.02 mg L−1. TheAl extracted by acid ammonium oxalate (Alo) provides anestimate of total non-crystalline Al (Blakemore 1978);extraction with sodium pyrophosphate (Bascomb 1968)provides an estimate of the organically bound Al (Alp);extraction with 0.5 M CuCl2 (Juo and Kamprath 1979)provides an estimate of organo-aluminium complexes oflow and medium stability (Alcu), and extraction with 0.5 MLaCl3, pH4 (Hargrove and Thomas 1981) provides anestimate of the most labile organic-aluminium complexes(Alla). Aluminium extracted with NH4Cl is exchangeableAl (Peech et al. 1947). The difference between Al extractedwith CuCl2 and Al extracted with LaCl3 (Alcula) representsorganic-aluminium complexes of intermediate stability(Urrutia et al. 1995); subtracting Alcu from Alp providesan estimate of the Al that forms highly stabile complexeswith organic matter (Urrutia et al. 1988) and subtractingAlp from Alo provides an estimate of inorganic non-crystalline Al (García-Rodeja and Macías 1987; García-Rodeja et al. 2004).

Aqueous extraction was carried out at a soil:solutionratio of 1:10, and the total soluble Al was determined bycolorimetry (pyrocatechol violet method: Dougan andWilson 1974; Shimadzu UV-1201V Spectrophotometer).

3 Data analysis

The data were analysed to determine mean values and rangesof variation. Simple correlation tests, linear regressions,comparisons of means, one-way analysis of variance and aTukey test (used to compare groups) were carried outfollowing the procedures in SPSS (version 11.5). Alldifferences were considered significant at p=0.05 and 0.01,which represent confidence levels of 95% and 99%,respectively.

4 Results and discussion

4.1 Soil pH

The pH (H20) ranged widely, from relatively low values(pH<3.3) to values close to 7 (Table 2).

Analysis of the pH revealed different acid–base conditionsfor the bulk and rhizosphere soil of the species considered atthe mine slope. Thus, the pH of the bulk soil was close to 7 forall three species, whereas the pH of the rhizospheric soil of theEricaceae (C. vulgaris and E. cinerea) was low (pH3.6–4.5),and the pH of the rhizospheric soil of S. atrocinerea was

similar to that of the bulk soil. Previous studies have shownthat when plants grow under adverse nutritional conditions,this may induce changes in soil pH, leading to increases ordecreases depending on the limitations of the substrate(aluminium toxicity, nutrient deficit etc.; Gadner et al.1983; Haynes 1990).

Several root-induced processes may modify the pH atthe rhizosphere, including charge balances associated withnutritional ionic absorption by roots, as cation uptake byroots leads to extrusion of H+ and anion uptake to releaseOH−, so that the charge balance in the system is maintained(Haynes 1990). Chelation of Al3+, Fe3+ and Ca2+ withorganic acids in the rhizosphere may reduce the pH ofthe rhizosphere and notably increase the tolerance to Al(Ma 2000). In this case, it appears that the Ericacea lowerthe soil pH around the roots, to around pH4–4.5, which insome cases implies a decrease of three pH units relative tothe bulk soil. This may be because C. vulgaris and E.cinerea are adapted to shallow, strongly acidic soils(Woolhouse 1981; Rodwell 1991). Corti et al. (2005) alsoreported that Erica arborea was able to colonise alkalinemarine deposits by acidifying the substrate via excretion oforganic acids through the roots.

On the other hand, the material in the mine dump isstrongly acidic (see Table 2). In this case, the environmentis favourable for the development of Ericaceae and thus thedifferences in acidity between the rhizospheric and bulk soilare less marked, as noted by Corti et al. (2005) for E.arborea grown in acidic media.

S. atrocinerea was only found on the mine slope wherethe pH was similar in the rhizospheric and bulk soils, inboth cases close to 7. This species is highly adaptable andis able to colonise many different types of environment(Ruíz de la Torre 1979; Díaz González and FernándezPrieto 1987; Silva-Pando and Rigueiro 1992), althoughthere are no reports of this species colonising strongly acidenvironments. This may indicate that the species is not ableto colonise such environments, which may explain theabsence of this species from the mine dump.

4.2 Organic C, total N and S

The mean percentage of organic C ranged from extremelylow (0.25%) to very high (8.80%) for this type of medium(see Table 2). The highest values correspond to therhizospheric soil in the dump, while the lowest valuescorrespond to the bulk soil in the dump.

If we consider the concentration of C in relation to thedistance from the root, there was a clear increase from thebulk soil to the rhizosphere in the mine dump. This was notso evident in the mine slope, in which the concentrations ofC in the internal rhizosphere (IR) and bulk soil (B) of C.vulgaris and S. atrocinerea were similar (see Table 2).

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Most of the organic C in the IR is attributed to manyfactors closely related to root activity, such as loss of apicalcells from the root, degradation of the fine roots, organiccompounds exudation and an abundant microbial popula-tion (Gobran et al. 1998; Fernández-Sanjurjo et al. 2000).Furthermore, most organic C in the dump is associated withlonger periods of colonisation by these species, in relationto the high degree of plant development in this materialwith regard to the mine slope.

The mean percentage of total N ranged between 0.01%and 0.53% (see Table 2), with the highest percentagecorresponding to the larger amounts of organic C. The positiveand highly significant correlation (r=0.85, p<0.01) betweenthese two variables appears to indicate that the organic N isthe principal N fraction in these soils. In the same way as forC, the mean N values were generally very low relative to thetypical values for the soil in the region. The percentage of Nin both the mine dump and slope was always higher in therhizospheric soil than in the bulk soil (see Table 2).

The concentration of total S measured in the minematerials (in both the slope and the dump; see Table 2) wasextremely high, since the values in natural soils intemperate climates range between 0.01% and 0.20%, withmore than 80% associated with the organic matter (Merinoet al. 1989; Brady and Weil 2002). In the material from theTouro mine, the total S and the organic matter were notsignificantly correlated (r=−0.09, p=0.74), indicating thatthe principal source of S is mineral, mainly Fe and Cusulphides (pyrite and chalcopyrite) present in the geologicalsubstrate. The total S and pH were significantly correlated(r=−0.63, p<0.01). Previous studies in mine dumps withsimilar characteristics revealed a close relationship betweenthe pH of the surface water and the concentration ofsulphate (Calvo da Anta et al. 1991). Oxidation of the metalsulphides present in the rock causes acidification of the soil

and an increase in the amount of sulphate. For this reason,the total S is considered an indicator of the potential aciditythat can be produced.

4.3 Fractions of Al in the soil solid phase

The concentration of total Al was similar in the slope(14,200 mg kg−1) and in the dump (13,765 mg kg−1; seeTable 1). The concentration of total non-crystalline Al (Alo)in the dump was 1,019 mg kg−1, which represents 3.6% ofthe total Al, whereas in the slope, the concentration was1,466 mg kg−1, which corresponds to 7.7% of the total. Inboth the mine slope and dump, the Alo was more abundantin the rhizosphere of the three species than in thecorresponding bulk soil (Table 3).

Acid oxalate is commonly used to dissolve short-rangeorder Al hydroxides and oxyhydroxides, Al bound toorganic matter and Al present in allophane and imogolite(Wada 1977; Theng et al. 1982). So that differences in thepH and/or the organic matter content of the rhizosphericand the bulk soil may explain the differences in the Alcontents in these two zones. In the dump, the highconcentration of Alo in the rizosphere may be explainedby the higher organic matter content, which may haveincreased Al complexation and the amount of Alo inrelation to the bulk soil. The highly significant correlationbetween Alo and organic matter (r=0.64, p<0.01) appearsto support this idea. However, in the mine slope, the strongacidity of the Ericaceae rhizosphere relative to the bulk soilmay result in a high rate of mineral weathering, with thesame overall effect. The concentrations of Alo in theEricaceae rhizosphere were much higher than in the S.atrocinerea rhizosphere (see Table 3), which may be relatedto a high degree of mineral weathering caused by theformer, due to the greater acidity of the rhizospheric soil.

pH (H2O) C (%) N (%) S (%)

Mean std Mean std Mean std Mean std

Dump B 3.7 0.2 0.25 0.04 0.01 0.00 0.36 0.07

ER C. vulgaris 4.0 0.1 1.70 0.67 0.07 0.02 0.43 0.06

IR C. vulgaris 4.0 0.1 3.71 1.13 0.15 0.05 0.43 0.05

ER E. cinerea 4.4 0.0 6.30 1.70 0.38 0.18 0.37 0.07

IR E. cinerea 4.3 0.1 8.83 0.75 0.53 0.21 0.30 0.01

Slope B 6.6 1.8 0.73 0.49 0.01 0.00 0.80 0.29

ER C. vulgaris 3.7 0.4 0.32 0.06 0.01 0.00 0.57 0.35

IR C. vulgaris 3.6 0.3 0.74 0.28 0.03 0.01 0.54 0.32

ER E. cinerea 4.7 0.1 1.00 0.03 0.02 0.01 0.84 0.01

IR E. cinerea 4.5 0.1 1.90 0.01 0.03 0.01 0.90 0.01

ER S. atrocinerea 6.3 1.4 0.47 0.15 0.02 0.00 0.93 0.09

IR S. atrocinerea 6.9 1.0 0.79 0.19 0.01 0.00 0.93 0.00

Table 2 pH (H2O), organic C,total N and total S in the bulksoil (B), external rhizospheric(ER) and internal rhizospheric(IR) soil of different plant spe-cies in the Touro mine dumpand slope

std standard deviation

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The aluminium extracted with sodium pyrophosphateestimates the total aluminium bound to organic matter(Bascomb 1968). In the bulk soil in the dump, the organicform of Al represents 3.2% of the total Al and 43.8% of theAlo, whereas in the slope, it represents 1.5% of the totaland 14.2% of the Alo. In this mine material, the totalaluminium bound to soil organic matter was positivelycorrelated with the soil organic matter (r=0.81, p<0.01)and negatively with pH (r=−0.48, p<0.01) and was higherin the Ericaceae rhizosphere (especially internal rhizo-sphere) than in the bulk soil (see Table 2). The greateracidity in the rhizosphere probably caused mobilisation ofAl, resulting in formation of organoaluminium complexes,favoured by the greater amount of organic matter in the rootenvironment. The Alp levels were lower than those reportedby other authors for Galician forest soils (Álvarez et al.1992, 2002; Camps et al. 2003) and for a lignite minedump, by Monterroso et al. (1994, 1998), possibly becauseof the lower organic matter content of the material in theTouro mine dump.

The aluminium extracted with copper chloride wasclosely correlated with organic matter (r=0.54, p<0.01).A similar trend was observed for Alcu and Alp (seeTable 3), and both forms were closely correlated (r=0.84,p<0.01). In all cases, the CuCl2 extracted less than half ofthe sodium pyrophosphate (between 23% and 49% of thesame). In Ericaceae, the abundance of intermediate andpoorly stable complexes decreased from the internalrhizosphere to the bulk soil, coinciding with a lowercontent of organic matter in the latter. The concentrationof these complexes in the internal rhizosphere was muchhigher in Ericaceae than in S. atrocinerea. This may be due

to the lower pH of the bulk soil in the former, which wouldhave favoured mobilisation of Al to the rhizosphere whereit would be precipitated or complexed by organic matter. Incontrast, the pH of the bulk soil of S. atrocinerea washigher, and thus the Al would not be mobilised because itwould be precipitated.

In the Ericaceae, the aluminium extracted with lantha-num chloride (Alla) was more abundant in the rhizosphere(see Table 3), which is consistent with the lower pH, andboth parameters were closely correlated (r=−0.64, p<0.01).The Al extracted with lanthanum chloride displayed asimilar pattern to the Al extracted with sodium pyrophos-phate and copper chloride, with which it was closelycorrelated (r=0.65 and 0.92, respectively, p<0.01). Lan-thanum chloride extracted between 2% and 21% of the Alextracted by sodium pyrophosphate, and between 5% and43% of that extracted by copper chloride. The concentrationof aluminium extracted with LaCl3 in the bulk soil and therhizosphere was lower than that reported by Camps et al.(2003) for Galician forest soils and by Monterroso et al.(1998) for the As Puentes mine dump, again coincidingwith a lower content of organic matter in the Touro mine.

Fractionation of the Al in the solid phase in both themine slope and the mine dump (Fig. 2) revealed apredominance of inorganic non-crystalline aluminium(Alop), unlike in Galician forest soils, in which Al-organic matter complexes predominate (Álvarez et al.1992, 2002). The Alop was closely correlated with the Alextracted by ammonium oxalate (r=0.91, p<0.01), and thisnon-crystalline mineral fraction represented between 33%and 92% of the total non-crystalline Al, with values higherthan 70% in 62% of the samples.

Table 3 Al in solid phase extracted with ammonium oxalate (Alo), sodium pyrophosphate (Alp), copper chloride (Alcu) and lanthanum chloride(Alla) in the bulk (B), external (ER) and internal (IR) rhizospheric soil for different plant species in the Touro mine dump (D) and slope (S)

Alo (mgkg−1) Alp (mgkg−1) Alcu (mgkg−1) Alla (mgkg−1) AlNH4 (mgkg−1)

Mean std Mean std Mean std Mean std Mean std

D B 1,019 120 446 39 185 14 57 4 194 14

ER C. vulgaris 1,436 138 560 229 203 11 50 0.8 162 5

IR C. vulgaris 1,392 82 622 264 203 27 58 4 187 13

ER E. cinerea 4,098 1,347 1,268 132 345 4 76 7 220 41

IR E. cinerea 4,033 1,134 1,782 70 414 104 102 22 304 82

S B 1,466 125 208 127 73 32 11 14 30 16

ER C. vulgaris 2,374 941 603 296 300 148 107 58 374 208

IR C. vulgaris 1,794 331 624 271 313 110 118 62 414 229

ER E. cinerea 3,091 45 234 67 67 45 25 9 88 15

IR E. cinerea 2,146 1,217 310 81 150 36 36 11 115 6

ER S. atrocinerea 1,794 212 193 64 71 22 4 2 5 9

IR S. atrocinerea 1,998 67 154 45 68 9 3 0.2 0.9 0.0

std standard deviation

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The most abundant fraction of the organoaluminumcomplexes was the highly stable Al (Alpcu; see Fig. 2),which was closely correlated with the total Al bound toorganic matter (r=0.98, p<0.01), and represented between38% and 81% of the Alp, with values higher than 55% in75% of the samples. The highly stable organoaluminiumcomplexes were followed in abundance by complexes ofintermediate stability (Alcula; see Fig. 2; between 13% and47% of the Alp), and poorly stable complexes were lessabundant (between 2% and 21% of the Alp).

In the Ericaceae, organoaluminium complexes of highand intermediate stability were more abundant in theinternal rhizosphere than in the bulk soil, and the totalconcentration of organoaluminium complexes was alsohigher in the former (see Fig. 2). These results appear toindicate that organic complexation of the aluminium inhighly stable complexes close to the roots is a mechanismthat prevents absorption of aluminium by the plant and thusits toxic effects. In this sense, some authors consider thatone of the principal mechanisms of plant tolerance to Alconsists of the exclusion of Al by root exudates (Barcelóand Poschenrieder 2002; Gallon et al. 2004; Wang et al.2006). Organoaluminium complexes are also scarce in thebulk soil and in the rhizosphere of S. atrocinerea, in whichthe pH is higher and organic matter is scarce.

The Al extracted with 1 M NH4Cl is considered readilyexchangeable (Peech et al. 1947). This type of Al forms

external sphere complexes at organic or inorganic exchangesites (Lin and Coleman 1960) and represents 1.4% of thetotal Al in the bulk soil in the dump and 0.2% of the bulksoil in the slope. The concentration of exchangeable Al washigher than that extracted with 0.33 M LaCl3 (see Table 3),and there was a close correlation between the amounts ofAl extracted with each extractant (r=0.99, p<0.01). Thisagain differs from what was observed in Galician forestsoils rich in organic matter, in which the LaCl3 alwaysextracted more Al (Álvarez et al. 1992, 2002). In the minesoils, characterised by a low content of organic matter, thelow amount of aluminium extracted with LaCl3 indicatedgreater specificity by organoaluminium complexes, whereasthe NH4Cl extracted both organic and inorganic forms ofaluminium. The highest concentrations of exchangeablealuminium were obtained in the rhizospheric soil of theEricaceae (see Table 3), coinciding with the lowest pHvalues measured in this zone. However, despite the acidityof these materials, the concentration of exchangeable Alwas lower than that obtained in the rhizosphere of theGalician forest species (Camps et al. 2003). These resultsappear to indicate that the Al resulting from mineralweathering is transformed into more stable forms, mainlyinorganic non-crystalline forms (see Fig. 2). At pH valuesclose to 7 (as in the S. atrocinerea rhizosphere and in thebulk soil around the Ericaceae on the mine slope), theconcentration of Al in the exchange complex was very low(see Table 3). Thus, the correlation between exchangeableAl and pH in these samples was highly significant (r=−0.83, p<0.01), and the correlation with the effective cationexchange capacity (eCEC) was also significant and nega-tive (r=−0.39, p<0.05). As regards the latter parameter, thehighest values were associated with less acid conditions(see Tables 2 and 4), as these materials contain componentsof variable charge, and the increase in pH caused anincrease in the negative charge of these colloids.

Aluminium saturation was also strongly influenced bypH, so that in the most acidic samples, such as the bulk soiland rhizosphere of the Ericaceae in the mine dump and therhizosphere of C. vulgaris in the mine slope, the percentageAl saturation in most samples was usually higher than 70%(see Table 4) and always higher than 20%, which isconsidered as the maximum amount acceptable for thedevelopment of species sensitive to Al (Mombiela andMateo 1984). Only Ericaceae species (and not S. atroc-inerea) grow in such media.

4.4 Aqueous aluminium

The mean concentration of Al in the aqueous extract rangedbetween 0.02 and 3.13 mg L−1 (see Table 4). The variationsin this element in the aqueous phase were mainly related tovariations in pH, which differed according to the type of

Fig. 2 (a) Forms of Al in the solid phase of the material in the Touromine slope and dump (b) and the external (ER) and internal (IR)rhizospheric soil associated with the three plant species. Alla,organoaluminium complexes of low stability; Alcula, Alcu–Alla(organoaluminium complexes of intermediate stability); Alpcu, Alp–Alcu (highly stable organoaluminium complexes); Alop, Alo–Alp(non-crystalline inorganic aluminium). Note different scales

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soil (rhizosphere or bulk soil) and the type of vegetation(see Tables 2 and 4).

The concentrations of total soluble aluminium weremuch lower than those reported for mine dumps affected bypyrite oxidation (Álvarez et al. 1993; Monterroso et al.1994, 1998) and even lower than those reported forGalician forest soil solutions (Álvarez et al. 1992, 2002,2005). The highest concentration of total soluble aluminiumwas observed in the Ericaceae rhizosphere (C. vulgaris andE. cinerea), which is where the lowest pH values wereobtained, while the concentration of Al in S. atrocinereawas very low, particularly in the bulk soil. In the mineslope, the total concentration of Al in solution was alwayshigher in the rhizosphere, coinciding with the lower pH.Other authors (Göttlein et al. 1999; Camps et al. 2003) alsoreported a higher concentration of soluble aluminium in therhizosphere in relation to the bulk soil in forest soils. In themine dump—where the variations in pH between the bulkand the rhizospheric soil were lower—there were nosignificant differences in total soluble Al between thesezones in relation to C. vulgaris, whereas higher concen-trations were obtained in the external rhizosphere of E.cinerea than in the bulk soil (see Table 3). In the latter case,the pH would not explain the differences in the concen-trations of soluble Al in the samples, and other process suchas lower uptake of Al through roots than input of Al bymass flow through the soil and/or higher concentrations oforganic ligands may explain the overall accumulation ofaqueous Al close to the root surfaces.

In general, at pH>5, the concentrations of Al were verylow in both the slope and the mine dump (Fig. 3), and theseparameters were negatively correlated (r=−0.53, p<0.01).This is consistent with the solubility of Al, whichprecipitates at between pH5 and 7. The total solublealuminium was also positively correlated with the ex-

changeable aluminium (r=0.43, p<0.01) and with theorganoaluminium complexes of intermediate stability (r=0.50, p<0.01) and those of low stability (r=0.45, p<0.01).The non-crystalline inorganic Al and the highly stableorganoaluminium complexes were not correlated with thedissolved Al. Some authors consider that highly stableorganoaluminium complexes are the principal source ofsoluble aluminium, while exchangeable Al regulates Alsolubility during soil acidification processes (Guo et al.2006). However, in the present study, the organic matterappeared to play an important role in withdrawing Al fromthe solution and fixing it in the highly stable complexes,which are more abundant in the rhizospheric zone.However, in these materials, organoaluminium complexesof medium and low stability and exchangeable Al may bethe principal sources of soluble Al. In these materials,mineral precipitation of Al in the form of poorly crystallinecomplexes may also be a valuable mechanism for control-ling soluble Al, a mechanism that is again more importantin the rhizosphere.

eCEC cmol(+)kg−1 Sat.Al (%) Total aqueous Al (mgL−1)

Mean std Mean std Mean std

Dump B 2.76 0.50 78 5.0 0.85 0.08

ER C. vulgaris 2.69 0.14 70 2.0 0.68 0.72

IR C. vulgaris 3.60 0.83 68 3.0 0.98 0.07

ER E. cinerea 10.33 5.45 24 1.2 3.13 1.02

IR E. cinerea 12.67 1.89 26 1.4 0.83 0.10

Slope B 17.30 10.27 3 0.5 0.02 0.02

ER C. vulgaris 5.60 1.72 74 4.0 2.17 2.27

IR C. vulgaris 6.07 2.33 76 3.5 2.24 1.66

ER E. cinerea 8.57 1.09 1 0.2 0.05 0.04

IR E. cinerea 6.98 0.03 18 0.8 0.38 0.06

ER S. atrocinerea 14.35 6.72 1 0.3 0.05 0.08

IR S. atrocinerea 17.52 8.90 0.5 0.1 0.10 0.04

Table 4 Effective cationexchange capacity (eCEC),saturation exchange complex inAl (Sat Al) and total aqueous Alin the bulk (B), external (ER)and internal (IR) rhizosphere fordifferent species in the Touromine dump and slope

std standard deviation

pH9 87 6 5 4 3

5.0

4.0

3.0

1.0

0

2.0

Total soluble Al (mg L-1)Fig. 3 pH vs. Al in solution inthe material in the Touro mineslope and dump

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5 Conclusions

The acid–base conditions in the Touro mine slope anddump were found to differ and ranged from close to neutraland acidic, respectively. The organic matter content wasvery low in both cases. Ericaceae were able to grow in bothtypes of material as they modified the pH of the rhizo-spheric soil from values close to neutral (mine slope) to lowvalues. In contrast, S. atrocinerea only grew in conditionswhere the pH was close to neutral values. The rhizosphericsoil was the richest in organic matter, mainly in the dumpmaterial, where the plants grew best.

The acidity and the high organic matter content of theEricaceae rhizosphere play a very important role in the Algeochemistry. The Al becomes mobilised in the acidicmedium of the rhizosphere, to form mainly highly stableorganoaluminium complexes, or precipitates as poorlycrystalline inorganic forms. These fractions may withdrawthe Al from the solution close to the roots, thus preventingabsorption of the element by the plants, and avoiding itstoxic effects. Therefore, despite the acidic nature of theenvironment under study, the concentration of dissolved Alwas low, with the principal sources being the exchangecomplexes and organic matter complexes of low andintermediate stability. The concentration of these organo-aluminium forms and of the exchangeable Al was lowerthan that obtained in Galician forest soils developed ongranite, because of the formation of highly stable organo-aluminium complexes and precipitation of non-crystallinemineral Al.

The almost neutral soil conditions in which S. atroc-inerea grows led to precipitation of inorganic Al, andtherefore, organoaluminium complexes, exchangeable Aland soluble Al were very scarce in the bulk and rhizo-spheric soil of this species.

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